Accepted Manuscript

Title: Phonological working memory in developmental

stuttering: Potential Insights from the neurobiology of
language and cognition

Authors: Andrew Bowers, Lisa M. Bowers, Dan Hudock,

Heather L. Ramsdell-Hudock

PII: S0094-730X(17)30103-1
DOI: https://doi.org/10.1016/j.jfludis.2018.08.006
Reference: JFD 5689

To appear in: Journal of Fluency Disorders

Received date: 29-9-2017

Revised date: 30-7-2018
Accepted date: 27-8-2018

Please cite this article as: Bowers A, Bowers LM, Hudock D, Ramsdell-Hudock HL,
Phonological working memory in developmental stuttering: Potential Insights from
the neurobiology of language and cognition, Journal of Fluency Disorders (2018),
https://doi.org/10.1016/j.jfludis.2018.08.006

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 Phonological working memory in developmental stuttering: Potential Insights
from the neurobiology of language and cognition

Andrew Bowers, Ph.D., CCC-SLP¹

albowers@uark.edu
**Corresponding author

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Lisa M. Bowers, Ph.D., CCC-SLP¹
lmbowers@uark.edu

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Dan Hudock, Ph.D., CCC-SLP²
hudock@isu.edu

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Heather L. Ramsdell-Hudock, Ph.D., CCC-SLP²
ramsdell@isu.edu

¹University of Arkansas

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Epley Center for Health Professions
606 N. Razorback Road
Fayetteville, AR 72701 N
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²Idaho State University
650 Memorial Dr. Bldg. 68
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Pocatello, ID 83201
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Highlights
 Behavioral findings implicate PWM or underlying cognitive processes in DS
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 Neurobiological models characterize PWM as a property of sensorimotor

integration
 Neural anomalies in DS are consistent with slower/mistimed sensorimotor
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integration
 Neural oscillations in PWM and sensorimotor integration should be examined
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Abstract:

The current review examines how neurobiological models of language and cognition
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could shed light on the role of phonological working memory (PWM) in developmental

stuttering (DS). Toward that aim, we review Baddeley’s influential multicomponent

model of PWM and evidence for load-dependent differences between children who
stutter (CWS) and adults who stutter (AWS) and typically fluent speakers (TFS) in

nonword repetition and dual-task paradigms. We suggest that, while nonword repetition

and dual-task findings implicate processes related to PWM, it is unclear from behavioral

studies alone what mechanisms are involved. To address how PWM could be related to

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speech output in DS, a third section reviews neurobiological models of language

proposing that PWM is an emergent property of cyclic sensory and motor buffers in the

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dorsal stream critical for speech production. We propose that anomalous sensorimotor

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timing could potentially interrupt both fluent speech in DS and the emergent properties

of PWM. To further address the role of attention and executive function in PWM and

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DS, we also review neurobiological models proposing that prefrontal cortex (PFC) and

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basal ganglia (BG) function to facilitate working memory under distracting conditions
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and neuroimaging evidence implicating the PFC and BG in stuttering. Finally, we argue
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that cognitive-behavioral differences in nonword repetition and dual-tasks are consistent

with the involvement of neurocognitive networks related to executive function and

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sensorimotor integration in PWM. We suggest progress in understanding the

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relationship between stuttering and PWM may be accomplished using high-temporal

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resolution electromagnetic experimental approaches.

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Abbreviation

DS developmental stuttering

CWS children who stutter

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AWS adults who stutter

PWM phonological working memory

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PFC prefrontal cortex

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BG basal ganglia

LTM long term memory

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PL phonological loop

VS

CE
visuospatial sketchpad

central executive
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EB episodic buffer
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TFS typically fluent speakers

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PWS People who stutter

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CWNS children who do not stutter

ERP event-related potential

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BGTC basal ganglia thalamo cortical

IFG inferior frontal gyrus

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PMC premotor cortex

PT planum temporal
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Spt sylvian parieto-temporal junction

STG superior temporal gyrus

STS superior temporal sulcus

MTG middle temporal gyrus

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 SFC state feedback control

CA conduction aphasia

BA Broddmann’s Area

IPL inferior parietal lobule

SPL superior parietal lobule

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PBWM basal ganglia model of working memory

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SMA supplemental motor area

ACC anterior cingulate cortex

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DIVA directions in auditory space to velocities in articulator space

GODIVA Gradient order DIVA model

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vMC ventral motor cortex

fMRI functional magnetic imaging

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A
SMG supramarginal gyrus
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DMN default mode network

DAN dorsal attention network

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VAN ventral attention network

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FPN fronto-parietal network

GMV gray matter volume

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MFG medial frontal gyrus

FA fractional anisotrophy
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PET positron emission tomography

ALE activation likelihood estimation

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A1 auditory cortex

OFC orbitofrontal cortex

SSI-4 Stuttering Severity Instrument – 4th Edition

EEG electroencephalography

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 MEG magnetoencephalagraphy

SMS Speech Motor Skill

Key

words

Phonological working memory

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Sensorimotor integration

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Executive function

Nonword repetition

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Dual-task

Stuttering

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1. Introduction
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A
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Developmental stuttering (DS) is a disorder of speech fluency associated with a

high recovery rate in preschool-age children who stutter (CWS) (>80%) and significant
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psychosocial and emotional consequences for those who persist into later childhood
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and adulthood. Multifactorial, dynamic models propose that DS is primarily a disorder

affecting the sensorimotor control of speech that is influenced by other psycholinguistic

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and cognitive-emotional factors (Smith, 1999; Smith & Weber, 2017; Starkweather,
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2002; van Lieshout, Hulstijn, & Peters, 2004). From this point of view, interacting

general cognitive capacities such as working memory, attention, and executive function
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play some as yet unclear role in the moment-to-moment variability and phenotypic

expression of stuttering in both CWS (Chang et al., 2017; Pelczarski & Yaruss, 2016;

Smith & Weber, 2017; Spencer & Weber-Fox, 2014) and adults who stutter (AWS) (Alm,

2004, Alm & Risberg, 2007; Kell, Neumann, & Behrens, 2017; van Leishout et al.,

5
2004). In particular, cognitive capacities known to support phonological working memory

(PWM), including phonological storage and the articulatory rehearsal of speech sounds,

have been implicated as a factor in preschool CWS that predicts subsequent recovery

or persistence (Mohan & Weber, 2015; Spencer & Weber-Fox, 2014). In CWS, PWM

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capacity may also be related to disturbances in cognitive-linguistic processing and to

variability in the expression of stuttering in contexts that load other cognitive processes

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supporting it, including attentional control and executive function both in CWS (Bajaj,

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2007; Eggers, De Nil, & Bergh, 2012; Kelly, & Walden, 2012; Jones et al., 2017; Usler &

Weber, 2015) and AWS (Alm, 2004; Alm & Risberg, 2007; Bajaj, 2007; Bosshardt,

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2006). As such, a better understanding of the cognitive processes underlying PWM has

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the potential to address long held questions about the nature of stuttering.
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Despite the potential significance of PWM, studies using tasks thought to load
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PWM in CWS and AWS have produced somewhat mixed results, and the underlying

mechanisms mediating recently reported differences remain unclear (Anderson &

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Wagovich, 2010; Anderson, Wagovich, & Hall, 2006; Byrd, McGill, & Usler, 2015; Byrd,
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Vallely, Anderson, & Sussman, 2012; Smith, Sadagopan, Walsh, & Weber-Fox, 2010).
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Perhaps as a consequence, while both CWS and AWS present with functional and

structural anomalies in both sensorimotor (Buchsbaum & D’Esposito, 2008; Buchsbaum

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et al., 2011; Hickok, Houde, & Rong, 2011; Jacquemot & Scott, 2006) and

neurocognitive networks implicated in PWM (Chang et al., 2017; Kell et al., 2017; Sitek
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et al., 2016), there have been no attempts to integrate existing cognitive-behavioral and

neuroimaging findings with neurobiological models of language and cognition. As such,

the aim of the current review is to examine how neurobiological models incorporating

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PWM in typical speech and language processing (Hickok & Poeppel, 2007; Jacquemot

& Scott, 2006) and executive function (D’Esposito, 2007; Hazy, Frank, & O’Reilly, 2007)

may shed light on underlying mechanisms mediating recent cognitive-behavioral studies

implicating lower PWM capacity in CWS (Anderson & Wagovich, 2010; Anderson et al.,

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2006; Spencer & Weber-Fox, 2014) and AWS (Byrd et al., 2015; Byrd, et al., 2012;

Smith et al., 2010). We argue that interpreting cognitive-behavioral findings in the

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context of neurobiological models may strengthen the relationship between underlying

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mechanisms affecting fluent speech production those underlying differences in PWM in

both CWS (Spencer & Weber-Fox, 2014) and AWS (Byrd et al., 2015; Byrd, et al.,

U
2012). In particular, we argue that interpreting cognitive-behavioral findings in the

N
context of neurobiological models may strengthen the relationship between underlying
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mechanisms affecting fluent speech production and those underlying differences in
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PWM.

Toward bridging the gap between cognitive-behavioral findings in DS and the

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neurobiology of PWM, section 2 reviews the relationship between DS and PWM

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capacity in the context of Baddeley’s influential multicomponent working memory model

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and behavioral findings from nonword repetition and dual-task paradigms that implicate

aspects of the executive function and phonological storage in CWS and AWS. In section
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3, we review neurobiological models proposing that PWM is an emergent property of

cyclic input and output buffers in the dorsal sensorimotor stream (Buchsbaum &
A

D’Esposito, 2008; Hickok et al., 2011; Jacquemot & Scott, 2006) and models proposing

that interactions between the prefrontal cortex (PFC) and basal ganglia (BG) mediate

working memory in attentionally demanding conditions (D’Esposito, 2007; Hazy et al.,

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2007). In support of differences in networks supporting PWM in DS, we review

neuroimaging evidence implicating large-scale networks in both CWS and AWS,

including PFC, BG, and dorsal stream sensorimotor regions. In section 4, we posit that

mistimed or ‘noisy’ dorsal stream sensorimotor integration previously proposed to cause

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stutter-typical disfluencies (i.e., part-word repetitions, prolongations, and blocks) may

also account for load-dependent differences on nonword repetition tasks in CWS and

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AWS. We further suggest that increased executive control of speech may play a

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modulatory role in regulating dorsal stream timing, as experience with stuttering

accumulates over the course of speech and language development. Lastly, in section 5,

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we propose that progress in understanding the cognitive processes underlying PWM in

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DS may be accomplished using noninvasive, high temporal resolution time-frequency
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methods in nonword repetition and dual-task paradigms.
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2. Phonological Working Memory in DS

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Much of the most recent work investigating aspects of PWM in DS references

Baddeley’s working memory model as an explanatory framework and thus a brief review
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of the model is worthwhile (Anderson & Wagovich, 2010; Anderson et al., 2006; Bajaj,

2007; Bosshardt, 2006; Byrd et al., 2015; Spencer & Weber-Fox, 2014). Currently, the
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model consists of four primary components proposed to interact with long-term memory

(LTM), which include the phonological loop (PL), visuospatial sketchpad (VS), central
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executive (CE), and episodic buffer (EB) (Baddeley, 2003, 2012). The PL is arguably

the component most relevant to the acquisition of speech and language and is

composed of two subcomponents, one component that provides temporary storage for

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phonological input known as the phonological store and a second to refresh the first via

subvocal articulatory rehearsal. Functionally, the PL is proposed to support new

phonological learning, facilitate the acquisition of new vocabulary, support second-

language acquisition, and potentially to influence action selection via subvocal rehearsal

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(Adams & Gathercole, 1995; Alloway et al., 2005; Baddley, 2012). The VS functions to

integrate spatial, visual, and kinesthetic information into a single representation for

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temporary storage. The CE component provides access to the other components and is

SC
broadly tasked with the control of attention to items to be held in working memory. The

latest and least studied addition to the model is the EB, a process proposed to have the

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capacity to store information in ‘chunks’ allowing it to exceed the capacity of the other

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components of working memory by interacting with LTM. In section 2.1, we review
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evidence from nonword repetition tasks implicating aspects of Baddely’s PL in CWS and
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AWS.
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2.1 A review of the evidence: Nonword repetition in DS

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A growing corpus of experimental and descriptive evidence implicates PWM

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differences in both CWS and AWS as compared to typically fluent speakers (TFS).

Much of the evidence linking PWM with stuttering has come from what are known as
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nonword repetition paradigms. Nonword repetition involves repeating words that

conform to phonological rules in the language but have no meaning (i.e., semantic
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content). In Baddeley’s model, such a task is thought to tap the storage component of

the PL without reliance on LTM for language (Gathercole, Willis, Baddeley, & Emslie,

1994). Following that reasoning, differences between people who stutter (PWS) and

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TFS on nonword repetition tasks in the absence of differences on verbal repetition tasks

would provide evidence favoring differences in PWM as distinct from LTM for semantic

content. Findings from nonword repetition tasks are of importance because nonword

repetition capacity in preschool children, as distinct from verbal working memory tasks,

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has been reported to predict subsequent recovery or persistence (Spencer & Weber-

Fox, 2014). In particular, it has been suggested that articulatory rehearsal and

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phonological storage may interact with other psycholinguistic capacities to influence

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persistence or recovery (Spencer & Weber-Fox, 2014). As such, in the sections that

follow, we first review studies reporting both significant group differences and a lack of

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differences in nonword repetition accuracy and subsequently discuss factors that may

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have led to nonsignificant findings in some studies. We suggest that the weight of the
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evidence implicates subtle, load-dependent differences in PWS from the preschool
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years up through adulthood.

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2.1.1 Nonword repetition findings in preschool-age CWS

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Early studies investigating nonword repetition in CWS provided somewhat mixed

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results with two studies in CWS (age range 2-8 years) reporting significantly lower

behavioral performance on children’s test of nonword repetition (Gathercole et al.,

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1994), a common measure of nonword repetition (Anderson et al., 2006; Hakim &

Ratner, 2004). In a follow-up study, Anderson and Wagovich (2010) reported that
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preschool CWS (3-5 years) who participated in both a picture naming task and a

nonword repetition task were significantly lower on the nonword repetition task only

compared to children who do not stutter (CWNS). Interestingly, the two groups did not

10
differ on a common measure of attention via parental report. However, within the group

of CWS a measure of ‘attentional focusing’ was positively correlated with nonword

repetition performance. More recently, Smith, Goffman, Sasisekaran, and Weber-Fox

(2012) did not detect group differences on a nonword repetition task in a group of

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preschool-age CWS (4-6 years). In that study, differences were only apparent for CWS

with concomitant speech-sound and/or language disorders, suggesting that other

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articulatory and cognitive-linguistic capacities may interact to influence performance on

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nonword repetition tasks. Further, although CWS without speech-sound/language

disorders did not differ on a measure of nonword repetition accuracy, they did show

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higher variability on indices of oral motor coordination (i.e., lip aperture variability),

N
suggesting that motor control of speech varied with nonword repetition load.
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In contrast to Smith et al. (2012), Spencer and Weber-Fox (2014) did find
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significant differences in nonword repetition performance between a preschool group of

CWS and CWNS (age range 3-5 years) with or without concomitant language and
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phonological disorders. Additionally, findings revealed that nonword repetition

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performance was significantly lower for CWS who persisted relative to those who
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recovered. Importantly, neither measures of expressive/receptive language nor

measures of working memory for words with semantic content were associated with
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recovery or persistence, suggesting a disassociation between verbal working memory

for words with semantic content and PWM. Most recently, Pelczarski and Yaruss (2016)
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reported statistically significant yet subclinical differences on a norm-referenced test of

nonword repetition in CWS (age range 5-6 years). Consistent with previous studies, no

differences were reported on a digit-span task, suggesting similar behavioral

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performance for words with semantic content. Taken together, the majority of nonword

repetition studies in in preschool CWS (5/6) suggest subtle, subclinical differences that

may also be related to or interact with articulation, phonology, and attentional

capacities. Further, studies that have also investigated aspects of verbal working

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memory via digit span or other memory tasks for words with semantic content also

suggest that reduced capacities for nonword sequences are not related verbal working

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memory capacity (Pelscarski & Yaruss, 2016) and do not appear to predict recovery or

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persistence (Spencer & Weber-Fox, 2014). Relevant details of the studies cited above,

including sample sizes, maximum syllable length of nonword stimuli, and effect sizes

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when reported are summarized in Appendix A (Table A.1).

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A
2.1.2 Nonword repetition findings in school-age CWS
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Relative to findings in preschool CWS, fewer published studies have investigated

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differences in school-age CWS and CWNS (age range 5-15 years). However, unlike
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studies of preschool CWS, only 3/6 studies report significantly lower performance in the

school-age CWS group when compared to CWNS. In the earliest report of nonword
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repetition in school-age CWS, Seery, Watkins, Ambrose, and Throneburg (2006)

reported no significant main effect between CWS and CWNS but did report a significant
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interaction between group and condition (i.e., nonword syllable length) at 5 syllable

nonword length. Bakhtiar, Abadm, and Panahi (2007) found no significant differences in
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nonword repetition accuracy between 12 CWS and 12 CWNS (age range 5-7 years)

using nonwords with a maximum length of 3 syllables. A retrospective study of 5

persistent CWS and 14 recovered CWS also reported no statistically significant group

12
differences on a nonword repetition task (Chon & Ambrose, 2007). Later, Weber-Fox et

al. (2008) reported that nonword repetition accuracy in a group of 10 CWS was similar

to a group of 30 CWNS in the same age range. In contrast to previous studies, Oyoun,

El Dessouky, Sahar, and Fawzy (2010) did find significant differences in nonword

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repetition accuracy between 30 CWS and 30 matched CWNS, suggesting that previous

studies using smaller sample sizes may not have detected a difference due to a lack of

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statistical power. A more recent study conducted by Sasisekaran and Byrd (2013) in

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CWS and CWNS ages 7-15, found no significant difference between CWS and CWNS

in overall nonword repetition accuracy and further found no differences in a nonword

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repetition condition requiring the omission of a target phoneme (i.e., phoneme elision).

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However, further subdivision of the CWS and CWNS into younger (7-11) and older (11-
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15) groups revealed a difference between the younger and older CWS that was not
M

present in the CWNS, suggesting that age may be a particularly important factor in

determining whether or not between group differences are detectable in school-age

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children. In summary, while most studies of school-age CWS have not reported
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between subject differences, those studies also used nonword stimuli of shorter syllable
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length than studies of preschool CWS. Further, the two studies that did detect overall

lower performance in CWS, either employed a 5 syllable length condition (Seery et al.,
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2006) or employed a larger sample size (Oyoun et al., 2010). As such, while it is as yet

unclear whether school-age CWS present with robust differences in nonword repetition
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accuracy, nonword repetition load, age, and sample size appear to be important factors

in determining whether a difference is detectable. A table summarizing findings from the

studies cited above is presented in Appendix A (Table A.2).

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2.1.3 Nonword repetition findings in AWS

Although most studies of school-age children have not reported significant

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differences in nonword repetition accuracy, most (5/7) studies in AWS have reported

lower behavioral performance. An early, preliminary study reporting significant

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differences in nonword repetition performance was consistent with significantly lower

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nonword repetition performance in AWS relative to TFS (Ludlow, Siren, & Zikria, 1997).

In a kinematic study of nonword repetition, Namasivayam and van Lieshout (2008)

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reported that AWS showed reduced practice effects reflected in higher movement
N
variability over several days when compared to controls. In another study of AWS who
A
were categorized with mild stuttering severity, Smith et al. (2010) found no differences
M

in accuracy on nonword repetition but did report group differences on a measure of

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inter-articulator coordination (i.e., labial aperture variability) with increasing length (1-4
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syllables) and phonological complexity of nonwords. While earlier studies had used

shorter nonword lengths, Byrd and colleagues (2012) investigated group differences at
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higher nonword loads (i.e., 7 syllables). A significant group by syllable interaction was

reported at the 7 syllable length nonwords only. In a subsequent study using a group of
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9 AWS and matched controls, Sasisekaran (2013) found no behavioral differences on

the Nonword Repetition Test (Dollaghan & Campbell, 1998) for 1-4 syllables but did find
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significant group differences using a measure of lip aperture variability on a nonword

reading task in which word lengths were varied between 6 and 11 syllables.

Subsequently, Sasisekaran and Weisberg (2014) reported that AWS showed an

14
increasing likelihood of nonword repetition errors with increasing length and

phonological complexity of nonwords (i.e., 6 syllables), suggesting that the load induced

by nonword stimuli may be a critical factor in detecting between group differences in

AWS.

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Building on findings from Byrd et al. (2012), Byrd et al. (2015) reported that

nonword repetition performance differed between AWS and TFS on 7 syllable nonwords

RI
but no differences were reported on 4 syllable nonwords. Additionally, decreases in

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performance were observed on a phoneme elision condition for 4 and 7 syllable

nonwords in which participants silently identified the nonword with a target phoneme

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omitted, strongly implicating phonological memory traces in the observed differences.

N
Finally, a recent report also demonstrated that AWS were less accurate at repeating
A
low-frequency iambic stress patterns in a 2-syllable nonword repetition task relative to
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higher-frequency trochaic stress patterns in the absence of auditory-orthographic cues,

suggesting that even at shorter syllable lengths phonological load manipulations may
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allow for the detection of group differences in behavioral accuracy (Coalson & Byrd,
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2017). Thus, collectively findings manipulating nonword repetition load suggest that
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AWS present with lower performance on nonword repetition tasks when PWM is heavily

loaded even into adulthood. A table summarizing findings from the studies cited above
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are presented in Appendix A (Table A.3).

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2.1.4 Implications of nonword repetition findings in CWS and AWS

In summary, the weight of the evidence implicates nonword repetition differences

from the onset of stuttering in the preschool years up through adulthood. First, while the

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majority of studies in preschool CWS have detected a group difference, some studies

that did not find significance may not have controlled for a number of influential factors.

In the only study of preschool CWS reporting no overall group difference in accuracy,

subgroups with language disorders and phonological disorders did present with

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significantly lower behavioral performance (Smith et al., 2012). By contrast, two other

subsequent studies found group differences in preschool CWS even without clinically

RI
significant language or phonological disorders (Pelczarski & Yaruss, 2016; Spencer &

SC
Weber-Fox, 2014). As noted by Pelczarski and Yaruss (2016), age, language ability,

and nonword stimulus factors such as length and complexity may not have been

U
adequately examined in previous studies. Further, most of the studies have included

N
preschool children that may subsequently recover, a factor that is likely to lead to higher
A
overall behavioral performance in CWS groups (Spencer & Weber-Fox, 2014). Given
M

the weight of the evidence and factors that may have affected findings in previous

studies reporting no group differences, nonword repetition capacity is strongly

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implicated in preschool-age CWS.

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In school-age children who stutter, while only 3 of 6 studies detected group

EP

differences, the studies that did employed larger sample sizes (Oyoun et al., 2010),

separated CWS into younger and older groups (Sasiskaran & Byrd, 2013), or detected
CC

differences only at longer nonword lengths (Seery et al., 2006). These findings suggest

that school-age CWS may present with higher PWM capacities than preschool CWS
A

and show differences primarily under high nonword repetition loads. That interpretation

is consistent with available evidence in AWS suggesting that the likelihood of detecting

differences in behavioral performance is heavily dependent on factors affecting nonword

16
repetition load (Byrd et al., 2012; Byrd, et al., 2015; Coalson & Byrd, 2017). Further,

kinematic differences, when measured, often show robust differences even at lower

loads in CWS and AWS (Sasisekaran, 2013; Sasisekaran & Weisberg, 2014; Smith et

al., 2010). Differences in kinematics in fluent nonword repetition have been taken as

PT
evidence of inefficient, immature, or compromised motor-control processes (Smith et al.,

2010) or as compensatory motor control processes in AWS that are related to

RI
compromised speech motor skill acquisition (Namasiayam & van Lieshout, 2008). It is

SC
also important to consider that, because differences in speech kinematics are present

during perceptually fluent nonword repetition in AWS, differences coordination,

U
amplitude, and slower adaptation over trials may also be interpreted as momentary

N
compensation for instabilities in speech motor control as a function of nonword
A
repetition load.
M

Despite variability in nonword repetition findings across studies, there are a

number of common themes. Interestingly, one common finding across recent studies is
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that preschool CWS tend to present with lower accuracy on nonword repetition tasks
TE

but do not present with differences on verbal repetition tasks with semantic content,
EP

suggesting a disassociation between verbal working memory and PWM early in DS

(Pelczarski & Yaruss, 2016; Spencer & Weber-Fox, 2014). One possible interpretation
CC

is that the disassociation may be related to compensatory processing in Baddeley’s EB

for words with semantic content that is not available for nonwords, suggesting that LTM
A

for language may play a compensatory role (Pelczarski & Yaruss, 2016). As noted in

Spencer and Weber-Fox (2014), successful nonword repetition requires at least intact

auditory-phonological processing, phonological analysis and storage, speech planning,

17
and ultimately execution. Those authors suggest that the amalgam of those processing

demands may index a fundamental process predictive of recovery and persistence.

Finally, given the results of Anderson and Wagovich (2010), it also seems likely that

some aspects of attention also interact with those processes in preschool CWS,

PT
suggesting that aspects of the CE may also be involved in observed differences.

Further, differences in school-age CWS and AWS have only been observed for higher

RI
nonword repetition loads, suggesting that aspects of executive function/attention may

SC
play an important role in observed differences. Differences in each process, including

the processing of speech sounds (Neef, et al., 2012; Saltuklaroglu, Harkrider, Thornton,

U
& Jenson, 2017), phonological encoding (Kolk & Postema, 1997), executive function/

N
attention (Alm, 2004; Alm & Risberg, 2007; Eggers, et al., 2012), and differences in
A
linguistic planning and execution (Howell & Au-Yeung, 2002; Kleinow & Smith, 2000),
M

have been proposed to play some role in DS (Bloodstein & Bernstein-Ratner, 2008). As

such, while nonword repetition appears to index an important process related to

D

persistence/recovery, the underlying mechanisms relating nonword repetition to

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stuttering are unclear.

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2.2 A review of the evidence: Dual-task performance in DS

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Given that the processes of attention and executive function likely interact with

the function of the PL, consideration of those capacities is critical when discussing the
A

potential role of PWM in DS. Behavioral evidence for the function of the CE in

Baddeley’s model is often examined through the lens of dual-task experimental

paradigms (Baddeley, 2012). In these dual-task experiments, participants complete

18
mental operations such as counting backwards while their performance is evaluated on

some target task. Baddeley and colleagues suggest that such tasks interrupt the

automaticity of the target task, placing load on aspects of cognition subserved by the

CE component (Baddeley, 2012). Following that reasoning, dual-task experiments could

PT
potentially provide a window into the link between PWM and aspects of cognition

relegated to the CE in PWS. Dual-task studies in AWS have investigated both aspects

RI
of target and secondary task performance as a measure of processing load along with

SC
effects on measures of stuttering. As such, in the sections below we review evidence for

differences in behavioral performance in dual-tasks along with evidence suggesting

U
effects on stutter-typical disfluencies.

N
A
2.2.1 Dual-task performance in school-age CWS and AWS
M

While a number of early dual-task studies investigated the performance of

D

distracting tasks on aspects of speech and language production in school-age CWS and
TE

AWS, those studies are difficult to interpret because it is unclear what cognitive

processes were engaged by secondary tasks. Early studies employed secondary tasks
EP

such as flickering lights, tracking a moving dot pattern, finger tapping, gross motor

activity, and tracking line patterns while CWS and AWS were engaged in various
CC

speech production tasks (Arends, Povel, & Kolk, 1988; Brutten & Trotter, 1985; Brutten

& Trotter, 1986). Two of the studies were conducted with school-age CWS and teenage
A

CWS (age range 6-17 years) and reported somewhat lower finger-tapping rates as

verbal task demands increased (Brutten & Trotter, 1985; Brutten & Trotter, 1986).

Subsequent studies in AWS have employed secondary tasks that were more readily

19
interpretable. In one early investigation, Caruso and Chodzko-Zajko (1994) reported

differences in the accuracy of a speaking (speech response latency and rate) while

AWS and matched TFS performed the Stroop color word task. More recently, Bosshardt

and colleagues conducted a series of studies in which AWS and matched TFS

PT
performed various speaking tasks along with a number of secondary tasks including

mental calculation, rhyme and semantic category decisions, and memorizing

RI
phonologically similar and dissimilar words (Bosshardt, 2002; De Nil & Bosshardt,

SC
2000). In the speaking tasks, group differences or interactions between task and group

showed differences in measures of inhalation rate or word duration. In sentence level

U
speaking tasks, decreases in the number of propositions were also found in dual-task

N
conditions relative to single task conditions (Bosshardt, 2002), suggesting that AWS
A
responded to task demands by reducing speech/linguistic output relative to TFS. In a
M

review of those studies, Bosshardt (2006) concluded that AWS compensate for the

effects of processing load in dual-tasks by reducing the ‘conceptual work’ of speech and
D

language production in an attempt to decrease stuttering.

TE

More recently, Smits-Bandstra and De Nil (2009) compared a group of AWS and
EP

TFS on repeated practice of ten syllable nonsense sequences while performing a color

recognition task. AWS demonstrated slowed speech sequence initiation over practice
CC

compared to the TFS group and decreases in syllable sequence reading accuracy.

Jones, Fox, and Jacewicz (2012) used a dual-task in which participants made rhyme
A

judgements while performing a letter recall task. While rhyme judgements did not show

group differences, reaction time, and letter recall decreases in accuracy for higher loads

(i.e., five letters) were observed. The differences in response time as opposed to

20
accuracy in rhyme judgements suggest that AWS may need more time to process

phonological information. Consistent with nonword repetition findings, apparent

behavioral differences were only detected when phonological processing was heavily

loaded. In accord with behavioral findings, a recent electrophysiological study also

PT
reported group differences in event-related potentials (ERPs) in a dual-task wherein

participants performed a tone discrimination task while at the same time naming

RI
pictures (Maxfield, Olsen, Kleinman, & Frisch, 2016). Whereas no differences in ERPs

SC
to tones were reported in the simple tone judgement task, ERPs were reduced in the

AWS group during the dual-tasks (i.e., phonological competition and lexico-semantic

U
conditions). Most recently, Eichorn, Marton, Schwartz, and Melara (2016) reported no

N
group differences in behavioral performance on a speaking task (narrative retell)
A
performed along with a range of tasks designed to load working memory/attention,
M

including a digit span and a spatial working memory task. While no differences in

behavioral performance were found, the AWS group did reduce the number of syllables
D

produced in the dual-tasks, suggesting that AWS adjusted speech and language to
TE

accommodate processing load. Taken together, the majority of findings support the
EP

notion that AWS make subtle adjustments to speech and language production to

accommodate processing limitations in dual-task compared to single task conditions.

CC

2.2.2 Dual-task effects on stuttering

A

While many dual-task studies have reported subtle adjustments in speech or

language, a smaller subset have also reported effects on stuttering in dual-tasks relative

to speaking tasks alone. Early studies employing a range of secondary tasks largely

21
unrelated to speech production or linguistic processing, found no effect on fluency or

more often decreases in stuttering under dual-task conditions (Bajaj, 2007). By contrast,

in one early study Caruso and Chodzko-Zajko (1994) reported increases in measures of

stuttering in the Stroop color-word task. Bosshardt and colleagues reported a complex

PT
relationship between dual-task conditions and measures of stuttered speech in which

secondary tasks that have minimal overlap with speech and language (e.g., mental

RI
calculation) result in reductions in stuttering (Bosshardt, 1999), while tasks that have

SC
ostensibly higher overlap with speech and language (e.g., memorizing phonologically

similar or dissimilar words) are associated with increases in stuttering (Bosshardt,

U
2002). Other conditions in which AWS reduce speech and language output in a

N
sentence generation task along with a secondary task (i.e., rhyme and category
A
decisions) were associated with no significant change in measures of stuttering in dual
M

relative to single task conditions, presumably because language output was reduced

(Bosshardt, 2002). In contrast with those findings, recent evidence has also
D

demonstrated decreases in measures of stuttering in dual-task relative to single task

TE

conditions. Vasic and Wijnen (2005) reported that stuttered speech reliably decreased
EP

in a dual-task in which AWS played video games while speaking. Similarly, Eichorn and

colleagues (2016) also reported decreases in measures of stuttering under dual-task

CC

digit-span and spatial-working memory tasks. Taken as a whole, the available evidence

suggests that the cognitive processes loaded in dual-task conditions may tap into a
A

cognitive resource that is related to both increases (Bosshardt, 2002; Caruso &

Chodzko-Zajko, 1994) and decreases in stuttering (Eichorn et al., 2016; Vasic & Wijnen,

2005) depending on the tasks or even compensatory strategies employed by AWS to

22
reduce task demands (Bosshardt, 2002). What is as yet unclear from dual-task studies

is what specific conditions or mechanisms are required to exacerbate or ameliorate

stuttering.

PT
2.2.3 Implications of dual-task findings

Collectively, findings in AWS implicate behavioral adjustments to speech and

RI
language output in dual relative to single task conditions. Despite findings suggesting

SC
dual-task adjustments to speech there are a number of unresolved issues. First,

although the evidence implicates differences in behavioral performance between AWS

U
and controls on a range of dual-tasks, there is much less evidence for differences in
N
CWS (Anderson & Wagovich, 2010; Brutten & Trotter, 1986). Although not a dual-task
A
study, Eichorn, Martin, and Pirutinsky (2017) recently reported that school-age CWS
M

have more difficulty with attentional control in a cognitive task measuring cognitive
D

flexibility, suggesting that aspects of executive function may indeed be ‘weak’ in CWS.
TE

Second, due in part to the wide array of secondary tasks employed in dual-task studies,

it is difficult to tease apart underlying mechanisms mediating differences in behavioral

EP

performance or stuttering. While the mechanisms are unclear, a number of explanations

have been offered. Smits-Bandstra and De Nil (2007) suggested that reduced dual-task
CC

performance is reflective of low levels of automaticity mediated by basal-ganglia-

A

thalamo-cortical (BGTC) loops. In that case, deficits or differences in the BGTC loops of

PWS cause decreases in new skill learning that do not become automatic with practice

at the same rate as TFS. Under dual-task conditions, attentional load further degrades

23
the process of automation over a number of trials, suggesting a neurophysiological link

between attentional resources, automation, and adaptive sensorimotor learning.

In more recent discussions, Maxfield and colleagues (2016) further propose that

attentional resources allocated to atypical linguistic processing related to covert

PT
behavior in AWS (e.g., word avoidance) may have significant effects on word retrieval,

speech-motor planning, and subsequent execution. Studies reporting greater fluency

RI
also make reference to attentional and working memory mechanisms (Eichornet al.,

SC
2016; Vasic & Wijnen, 2005). More specifically, Eichorn et al. (2016) interpret findings of

decreased stuttering in dual-task conditions as consistent with the Matched Filter

U
Hypothesis (Chrysikou, Weber, & Thompson-Schill, 2014). According to that framework,

N
top-down attentional control can be detrimental for tasks that require relatively
A
automatic motor performance (i.e., procedural tasks). According to Eichhorn et al.
M

(2016), when working memory/attentional resources are otherwise engaged and top-

down control of speech is reduced, more automatic mechanisms (e.g., subcortical

D

mechanisms) facilitate speech production. Thus, the effects of top-down attentional

TE

control on speech in dual-tasks is consistent with mechanisms mediating enhanced

EP

fluency in some contexts (Eichorn et al., 2016) and deleterious effects in others

(Bosshardt, 2006; and see Metten et al., 2011), perhaps depending on the direction of
CC

attention or the extent to which dual-tasks share cognitive resources for speech and

language.
A

2.2.4 Implications of nonword repetition and dual-task findings

24
 Collectively, nonword repetition and dual-task findings support the notion that

limitations on the cognitive capacities underlying PWM may be related to stuttering from

the preschool years into adulthood. First, the majority of studies in preschool CWS

suggest a load dependent vulnerability to cognitive factors also known to load PWM,

PT
including phonological analysis, temporary storage, and speech motor planning prior to

nonword repetition. While differences in behavioral accuracy are likely to be subclinical

RI
(Pelczarski & Yaruss, 2016) and may interact with other cognitive-linguistic capacities

SC
(Anderson & Wagovich, 2010; Smith et al., 2012), they are also related to subsequent

recovery and persistence (Spencer & Weber-Fox, 2014). Further, load-dependent

U
differences are present even in older school-age CWS and AWS. As such, the

N
behavioral evidence from nonword repetition paradigms suggest subtle, load dependent
A
limitations on what Baddeley described as the PL in both CWS and AWS relative to
M

TFS. We suggest that this difference in PWM capacity may be of importance because

the processing demands required in nonword repetition appear to be related to

D

persistence and recovery (Spencer & Weber-Fox, 2014; Mohan & Weber, 2015) and
TE

may interact with other psycholinguistic processes (e.g., syntax) over the course of
EP

language development to influence the expression of stuttering (Usler & Weber-Fox,

2015),
CC

Second, while it is unclear from nonword repetition studies how PWM may be

related to overt stuttered moments, dual-task studies suggest that loading aspects of
A

attention in speech production is associated with effects on stuttered speech, especially

under conditions in which PWM is loaded (Bosshardt, 2002). However, it also appears

that effects on stuttering sensitively depend on study conditions, with some studies

25
providing evidence of increases in stuttering (Caruso & Chodzko-Zajko, 1994; Maxfield

et al., 2016) and others paradoxically reporting decreases in stuttering (Eichhorn et al.,

2016; Vasic & Winjin, 2005). Stutter-typical disfluencies may vary based on the internal

attention to speech and language production or the extent to which secondary tasks

PT
load overlapping processes required for speech and language processing (Bosshardt,

2006). Thus, while the underlying mechanisms mediating dual-task findings are unclear,

RI
they do implicate aspects of what Baddeley described as the CE and PL in the

SC
modulation of language production and stuttering under high cognitive-load conditions.

We suggest that those findings are important because it is likely that AWS also

U
experience greater cognitive-linguistic loads in more naturalistic communicative

exchanges when compared to TFS. N

A
M

3. PWM in neurobiological models of language and cognition

D

It is important to consider that, if CWS and AWS do present with differences in

TE

executive control interacting with a phonological loop, then the neurocognitive networks

identified in CWS and AWS should be consistent with neurobiological models proposing
EP

mechanisms to account for those same cognitive capacities. Toward bridging the gap

between cognitive-behavioral findings and neurobiological models, the sections below

CC

describe models of language proposing that PWM is an emergent property of sensory

and motor regions within the perisylvian network (Buchsbaum & D’Esposito, 2008;
A

Hickok & Poeppel, 2007; Hickok et al., 2011; Majerus, 2013). In addition, because DS is

associated with differences in attentional control/executive function in both CWS and

AWS, we also describe a model proposing that interactions between the prefrontal

26
cortex (PFC) and basal ganglia (BG) are also critical for working memory under

distracting or attentionally demanding conditions (Hazy et al., 2007). Finally, we review

brain imaging findings that implicate differences in large-scale networks supporting

executive function/attentional control, PWM, and speech processing in the

PT
pathophysiology of both CWS and AWS. Taken as a whole, we suggest the networks

implicated in the pathophysiology of stuttering are consistent with load dependent

RI
differences in behavioral accuracy in nonword repetition and dual-tasks.

SC
3.1 PWM in the dual-stream model of language

U
While DS is most often associated with functional and structural differences
N
within perisylvian regions (Etchell, Civier, Ballard, & Sowman, 2018), it has only been in
A
the last decade that neurobiological frameworks have proposed that perisylvian regions
M

support PWM (Buchsbaum & D’Esposito, 2008; Herman, Houde, Vinogradov, &
D

Nagarajan, 2013; Jacquemot & Scott, 2006; Majerus, 2013). In an early model,
TE

Jacquemot and Scott (2006) proposed that auditory-sensory regions and premotor

regions act as cyclic input and output buffers respectively allowing for phonological
EP

storage, suggesting a link between sensorimotor mechanisms in natural speech

production and those involved in PWM. More recently, Hickok and Poeppel’s (2007)
CC

‘dual-stream’ model of speech and language processing also proposes that interactions

between premotor, auditory-sensory, and audiomotor regions account for the emergent
A

properties of PWM. According to their dual-stream model, a left hemisphere dominant

dorsal stream, including aspects of the posterior inferior frontal gyrus (IFG), premotor

cortex (PMC), and the planum temporale (PT) at the parietotemporal boundary (Spt),

27
mediate the conversion of input from auditory-phonological regions to articulatory output

in the IFG/PMC regions. In the model, the primary auditory cortex along the superior

temporal gyrus (STG) is involved in spectrotemporal processing bilaterally and a left

dominant region along the superior temporal sulcus (STS) is involved in retrieving

PT
phonological codes. A bilateral ventral stream in the anterior and more posterior aspects

of the middle temporal gyrus (MTG) and inferior temporal sulcus are more heavily

RI
involved in processing receptive language and mediate lexical access (see Hickok &

SC
Poeppel, 2007 for visual representation). Finally, although the dorsal and ventral

streams are proposed to interact in language formulation and processing, it is as yet

U
unclear how and when the two streams interact to allow for speech and language

production in naturalistic contexts. N

A
In the dual-stream model, short-term phonological memory (hereafter referred to
M

as PWM) is proposed to emerge from interactions between auditory-phonological

regions in the STS, audiomotor mapping in the PT, and premotor regions of the dorsal
D

stream responsible for motor programming and execution (Buchsbaum & D’Esposito,
TE

2008; Hickok, Buchsbaum, Humphries, & Muftuler, 2003). In particular, a region of the
EP

PT at the sylvian parieto-temporal junction (i.e., area Spt) is active during tasks in which

covert rehearsal is required for maintenance of phonological information in working

CC

memory. The same region is active for auditory encoding, subvocal rehearsal, and overt

production in a number of tasks, including multisyllabic nonword repetition (Buchsbaum,

A

Hickok, & Humphries, 2001), ‘jabberwocky’ phrase repetition, and even covert rehearsal

of piano melodies (Hickok et al., 2003). Finally, the dorsal stream network also mediates

behavioral performance on common clinical nonword auditory processing tasks, even in

28
the absence of a requirement for production, strongly suggesting that the dorsal stream

mediates PWM even when execution is not required (Perrachione, Ghosh, Ostrovskaya,

Gabrieli, & Kovelman, 2017). Thus, the dual-stream model suggests that the integration

of sensory and motor representations are critical both for speech production and the

PT
emergent properties of PWM. From this point of view, damage or disrupted input to the

left hemisphere dorsal stream would be expected to cause both effects on speech

RI
production and tasks that load PWM.

SC
3.2 Disorders of dorsal stream sensorimotor integration and PWM

U
Working from a dual-stream model of language and a state feedback motor
N
control (SFC) model, Hickok and colleagues (2011) proposed that both DS and an
A
acquired language disorder known as conduction aphasia (CA) are consistent with
M

dorsal stream disruptions affecting speech production. From that point of view,
D

individuals with CA have particular difficulty with word repetition related to impaired
TE

PWM caused by damage to are Spt (Buchsbaum et al., 2011; Hickok et al., 2011). For

individuals with CA, phonological errors in natural speech production occur relatively
EP

infrequently but are more likely when producing multisyllabic and low frequency words,

suggesting parallels between the loci of phonological errors in CA (Buchsbaum &

CC

D’Esposito 2008; Buchsbaum et al., 2011) and similar linguistic factors known to

influence the likelihood of stutter-typical disfluencies in DS (Howell & AuYeung, 1995,

A

Howell & AuYeung, 2002). Thus, in the same way that individuals with CA experience

load-dependent phonological errors in speech production and poor word repetition,

29
PWS experience load-dependent disfluencies and load-dependent effects in nonword

repetition tasks.

According to an SFC model of speech production, for accurate speech

production to occur, an inhibitory model of the intended sensory consequences (i.e., a

PT
forward model) is generated in premotor and motor regions (i.e., a motor-phonological

system), while an excitatory, corrective model is generated in somatosensory and

RI
auditory regions (i.e., a sensory-phonological system) (Hickok et al., 2011; Houde &

SC
Nagarajan, 2011). An audiomotor translator in area Spt mediates the conversion of

motor and sensory phonological information. When the inhibitory forward model is

U
accurate, no correction is needed and the two models are considered to cancel out.

N
However, in instances wherein an error in the forward model is detected, excitatory
A
corrective models are sent back to the PMC and primary motor areas for correction prior
M

to overt production (Hickok, 2012). In people with CA, damage to Spt is proposed to

disrupt forward predictions sent from motor-phonological areas to the auditory-

D

phonological regions, causing errors in the internal monitoring process. However,

TE

because the auditory-phonological regions are intact, a person with CA is nonetheless

EP

able to detect the error and engages in repeated and often unsuccessful attempts to

correct it.
CC

By contrast, in DS the motor-phonological and sensory-phonological systems are

intact but the audio-motor translator provides ‘noisy’ or high variance input to the
A

auditory-phonological system (Hickok et al., 2011). Due to this noisy input, forward

sensory predictions generate estimates of vocal-tract states and auditory-phonological

targets that cause an invalid error signal to be sent back to the motor-phonological

30
system. The behavioral consequence of this noisy translation is a predict-correct loop

that, under conditions of high sensorimotor ‘load,’ results in overt disfluencies (e.g., part-

word repetitions). Further, Hickok and colleagues (2011) predicted that errors in

sensorimotor mapping should be proportional to the load on the network. From this

PT
point of view, higher sensorimotor ‘load’ would be expected on low frequency words,

multisyllabic words, or potentially in situations taxing other systems related to speech

RI
such as when speaking under time-pressure. Because nonword repetition tasks rely

SC
heavily on the same network, one prediction of this approach would be that high

variance sensorimotor integration would also result in load dependent errors in

U
repetition as reported in both preschool CWS at lower loads (Pelczarski & Yaruss, 2016;

N
Spencer & Weber-Fox, 2014) and older CWS and AWS at higher loads (Byrd et al.,
A
2012; Byrd et al., 2015; Coalson & Byrd, 2017; Sasisekaran, 2013). As such, the above
M

described mechanisms provide a potential neurophysiological link between internal

models of motor control proposed to explain the emergence stutter-typical disfluencies

D

(Brown, Ingham, & Ingham, 2005; Guenther, Ghosh, & Tourville, 2006; Hickok et al.,
TE

2011; Max, Guenther, & Gracco, 2004; Tian & Poeppel, 2012) and the dorsal
EP

sensorimotor stream proposed to support PWM for learning new words, new

phonological representations, and errors in natural, connected speech production

CC

(Buchsbaum & D'Esposito, 2008; Hickok et al., 2011; Jacquemot & Scott, 2006; and see

Page, Madge, Cumming, & Norris, 2007).

A

3.3 PWM in neurobiological models of executive control

31
 While a dorsal stream deficit in DS is plausible, it is unclear from a dual-stream

model alone how attention and executive function under high load conditions might

interact with the dorsal stream. Whereas Baddeley’s cognitive model proposes

interactions between the CE and PL, other models suggest that task relevant

PT
information is not maintained in dedicated storage areas but as a subset of processes

that are in the focus of attention (Cowan, 1999; Cowan, Elliott, Saults, Morey, & Mattox,

RI
2005). A number of neurobiological accounts have implicated the dorsolateral prefrontal

SC
cortex (BA 46/BA 9) and ventrolateral PFC regions (BA 47/45) in attentional capacities

along with the inferior parietal lobule (IPL) and superior parietal lobule (SPL) (e.g.,

U
Baddeley, 2003; Buchsbaum & D’Esposito, 2008; Majerus, 2013; Nee, Brown, Askren,

N
& Berman, 2013). Evidence from neuroimaging studies examining working memory in
A
the contexts of visual, auditory, and affective stimuli also suggest that PFC regions
M

interact with other networks depending on the modality of the stimulus to be held in

working memory (e.g., visual vs. auditory). In this way, the same networks involved in
D

sensorimotor representations of the object to be recalled maintain it via interactions with

TE

attentional and executive control regions in the PFC (D’Esposito, 2007).

EP

Other neurocomputational approaches emphasize interactions between the PFC

and BG in working memory performance under attentionally demanding or distracting

CC

conditions (Baier, Karnath, Dieterich, & Birklein, 2010; McNab & Klingberg, 2008;

Voytek & Knight, 2010). According to the prefrontal cortex and basal ganglia model of
A

working memory (PBWM), the BG provides a ‘go’ or ‘nogo’ signal to the PFC to

modulate information relevance while more primitive BG to premotor connections (e.g,

supplemental motor area and anterior cingulate cortex) modulate action selection and

32
execution (Hazy et al., 2007; Mink, 1996). In the PBWM computational model, dynamic

gating via midbrain structures is learned via reinforcement mechanisms thought to rely

on dopaminergic systems, while PFC representations are updated using Hebbian and

error-driven learning mechanisms. Bidirectional excitatory connections from the

PT
thalamus to the frontal cortex are inhibited by tonically active neurons in the substantia

nigra pars reticulata. In turn, the substantia nigra is disinhibited by ‘go’ neurons in the

RI
dorsal striatum, allowing for disinhibition of the frontal cortex and gating of working

SC
memory in the PFC under distracting conditions. This process allows the PFC to

maintain only relevant information in working memory under distracting conditions while

U
the dopaminergic systems involved in learning and motivation (including the bilateral

N
amygdala) evaluate the potential reward value of actions and goals maintained in the
A
PFC, thereby modulating future actions. Finally, the model proposes an output-gating
M

mechanism that can determine which of a set of actively maintained representations

should be selected for motoric planning and output.

D

Working from the PBWM model, it is reasonable to propose that PFC-BG

TE

connectivity could modulate action selection and thus dorsal stream sensorimotor
EP

control networks in PWS as a lifetime of experience with stuttering accumulates. The

model also provides a potential mechanism by which neural learning could affect the
CC

plasticity of networks involved in speech production, leading to variability in the

expression of stuttering as new experiences accumulate. In such cases, learned

A

behaviors such as fluency enhancing motor control strategies, anticipation of difficult

social situations, and covert attempts to avoid or substitute words would be modulated

by ever evolving connections between the PFC, BG, and the dorsal sensorimotor

33
stream. As such, in the sections following, we discuss theoretical frameworks

implicating sensorimotor integration and speech-motor timing early in the development

of stuttering and neuroimaging evidence supporting a role for PFC and BG structures in

connection with dorsal stream networks in CWS and AWS.

PT
RI
3.4 PFC, BG, and dorsal stream sensorimotor timing

SC
While interactions between executive control in the PFC, BG, and dorsal regions

involved in phonological ‘storage’ appear to play a role in DS, one potential problem is

U
that the mechanism underlying ‘noisy’ sensorimotor integration is somewhat
N
underspecified. For example, it is unclear how a difference in dorsal stream processing
A
might lead to stutter-typical disfluencies in PWS as opposed to the phonological errors
M

observed in CA. There is not strong support for the notion that phonological errors of the
D

kind observed in CA covary with stuttering (Nippold, 2002; Nippold, 2012), suggesting
TE

that the sensorimotor errors in PWS are likely to involve a different process. One

possibility is that, rather than phonological errors caused by damage to the Spt region
EP

as in CA, disrupted sensorimotor integration is instead a matter of inaccurate

coordinative timing mediated by the dorsal sensorimotor stream and connections with
CC

subcortical structures also implicated in speech-motor timing (e.g., the BG and

cerebellum). While findings in AWS regarding timing in non-speech motor control have
A

been variable, the notion that stuttering is primarily a disorder of timing or coordination

for speech production has long been the subject of theoretical proposals (Alm, 2004;

Etchell, Johnson, & Sowman, 2014; Kent, 1984; Perkins, Kent, & Curlee, 1991; Smith &

34
Weber, 2017; Van Riper, 1982). As such, subtle timing differences in sensorimotor

integration could potentially account for the process disrupting both fluent speech

production in PWS and differences in tasks loading PWM. In the sections below, we

describe neurobiological frameworks and findings implicating speech-motor timing

PT
networks in sensorimotor integration and internal models of motor control.

RI
3.4.1 Neurobiological frameworks supporting sensorimotor timing

SC
differences in DS

Similar to the dorsal stream SFC model described in section 3.2, connections

U
between the BG and frontotemporal-parietal networks involved in sensorimotor timing
N
for speech have also been used to explain a wide range of phenomena in stuttering
A
(Alm, 2004; Alm & Risberg, 2007; Civier, Bullock, Max, & Guenther, 2013; Etchell et al.,
M

2018; Wu, Maguire, Riley, Lee, Keator, & Tang, 1997). In an influential proposal, Alm
D

(2004) posited that differences in dopamine receptor concentrations in the BG early in

TE

speech motor development cause sensorimotor instabilities in CWS. According to Alm

(2004), unstable timing cues provided by the BG are read out to the supplemental motor
EP

area (SMA) for subsequent movement sequencing, eventually resulting in repetitions or

prolongations of movement to compensate for the deficit. Drawing on Goldberg's dual-

CC

premotor hypothesis, Alm (2004) suggested a medial premotor system (SMA and BG) is
A

more heavily involved in overlearned, automatic, and internally initiated movements

whereas the lateral premotor system (lateral PMC and cerebellum) is more heavily

involved in the control of externally cued, less automatic, and novel movement patterns.

The increased fluency well-known to result from altered auditory feedback, choral

35
speech, and rhythmic speech (e.g., speaking to a metronome) were proposed to be the

result of a shift from a compromised medial premotor system to that of an

uncompromised (or less compromised) lateral premotor system. In addition to fluency

enhancing effects, it was also proposed that attention to compensation for sensorimotor

PT
instability may shift internal timing cues from the medial to lateral premotor system when

speech production is less automatic or overlearned (e.g., when using fluency shaping

RI
techniques). More recently, Alm and Risberg (2007) also proposed that situational

SC
variability related to social cognition mediated by the polar medial PFC (BA10), anterior

cingulate cortex (ACC), and SMA could be related to situational variability in stuttering

U
during social interactions. From that point of view, the medial PFC through connections

N
with the BG and premotor regions may modulate motor control depending on social-
A
cognitive demands. Thus, connections between the PFC, BG, and frontotemporal-
M

parietal networks are implicated in modulating sensorimotor control and speech fluency

depending upon context.

D
TE

3.4.2 Neurocomputational modeling evidence supporting a link between BG

EP

timing networks and internal models

In addition to PFC and BG timing networks proposed by Alm (2004), elevated

CC

dopamine levels are also implicated in interaction with an overreliance on sensory

A

feedback mechanisms derived from internal models of motor control (Civier, Tasko, &

Guenther, 2010; Civier et al., 2013; Max et al., 2004). In a computational modeling

study, Civier et al. (2010) used the directions in auditory space to velocities in articulator

space (DIVA) computational model to simulate an inefficient feedforward model, forcing

36
the model to rely on time-lagged auditory feedback control. The results suggested that

when accumulating errors between the feedforward and feedback models were large

(indexed by formant transitions for the auditory targets), self-repair was initiated in the

form of a ‘reset’ or syllable repetition. A second modeling study used the gradient order

PT
DIVA model (GODIVA) to simulate two proposed brain differences in AWS, a white-

matter anomaly in the ventral motor cortex (vMC) and elevated dopamine levels (Civier

RI
et al., 2013. Those authors reported that whereas elevated dopamine levels affecting

SC
the BG could account for syllable initial disfluencies, the white-matter anomaly could

only account for disfluencies on syllables in the middle or later in an utterance,

U
suggesting that the two potential causes of disfluency likely interact. Computational

N
modeling findings using the GODIVA model have recently been extended to nonword
A
syllable repetition (Markiewicz & Bohland, 2016) with more specitific descriptions of the
M

functional role of various input and output buffers in syllable production and their

interaction with the BG (see Bohland, Bullock, and Geunther, 2010). Taken together,
D

compucational modeling findings do suggest a link between the functional role of the
TE

BG in speech production and internal models of motor control.

EP

The potential link between timing cues for speech mediated by the BG and

internal model proposals is of interest for explaining the relationship between DS and
CC

PWM because timing in internal models of motor-control have also been implicated in

PWM (Herman et al., 2013). Similar to neurobiological models of speech motor control,
A

the maintenance of phonological traces between motor-phonological and sensory-

phonological regions would be expected to require timely cyclic interactions (Jacquemot

& Scott, 2006; Hickok et al., 2011; Herman et al., 2013). That is, cyclic activation and

37
suppression between motor and sensory buffers must be maintained prior to execution

both in repetition tasks requiring maintenance of phonological traces and in natural

speech production (Herman et al., 2013; Jacquemot & Scott, 2006; and see Page et al.,

2007). As such, one likely source of variance in sensorimotor input to the left PT region

PT
in PWS is generally slowed or mistimed information for phonological/lexical targets with

subsequent effects on execution. Further, it is likely that areas of the PFC modulate

RI
sensorimotor timing and dorsal stream coordination depending on context (Alm &

SC
Risberg, 2007). To explore that possibility, in sections following we review functional

and structural brain imaging evidence implicating connectivity in large-scale

U
neurocognitive networks in CWS and AWS consistent with differences in the

N
connectivity of PFC, BG and dorsal sensorimotor regions implicated both in speech
A
production and PWM.
M

3.4.3 Functional imaging findings in CWS

D
TE

One source of evidence for differences in large-scale neurocognitive networks in

CWS comes from functional imaging studies. Recent functional magnetic resonance
EP

imaging (fMRI) studies implicate differences in activation or connectivity of large-scale

networks related to attention/executive function and timing for the sensorimotor control
CC

of speech (Etchell et al., 2018). In resting-state recordings of children 3-9 years of age,

hypo-connectivity motor (IFG/ primary motor cortex/PMC), auditory (MTG/STG), and

A

somatosensory association regions (e.g., the supramarginal gyrus; SMG) have been

reported, suggesting that a decreased capacity for timing emerges early in intrinsic

BGTC networks. Further, hyperconnectivity in the right superior frontal gyrus and

38
putamen was also found in CWS relative to CWNS, implicating connections between

the PFC and BG (Chang & Zhu, 2013). Another recent study of cortical connectivity with

the BG (i.e., the putamen) during rhythm perception also found decreased connectivity

with the left PMC, left STG, SMA, and cerebellum that was also related to lower

PT
behavioral performance in CWS relative to CWNS (Chang, Chow, Weiland, & McAuley,

2016). In a study of resting-state cerebral blood flow of CWS and AWS, the CWS were

RI
reported to have lower perfusion in Broca’s area and the superior frontal gyrus relative

SC
to TFS that inversely correlated with stuttering severity (Desai et al., 2016).

Most recently, differences in metabolite ratios between school-age and

U
adolescent CWS and TFS (age range 5-17 years) within wide-spread executive

N
function/attentional networks, speech sensorimotor control networks, and networks
A
involved in memory were also reported using proton chemical shift imaging (O’Neill et
M

al., 2017). Finally, a recent longitudinal study in CWS reported anomalous connectivity

in the resting-state between what is known as the default mode network (DMN), dorsal
D

attention network (DAN), ventral attention network (VAN), fronto-parietal network (FPN)
TE

(including the PT region), and somatomotor network, further implicating broader

EP

attentional, audiomotor, and somatomotor regions in the pathophysiology of stuttering

early in speech and language development (Chang et al., 2017). More importantly,
CC

anomalous connectivity between the DMN, DAN, VAN, and frontoparietal network also

predicted later persistence in CWS (Chang et al., 2017). Thus, taken together,
A

functional neuroimaging findings implicate large-scale neurocognitive networks involved

in, attention, speech-motor timing, and sensorimotor integration early in the preschool

and school-age years. Because the cognitive capacities implicated in those networks

39
are also related to working memory brain activation and behavioral performance (Zhu et

al., 2013), those findings are consistent with differences in neurocognitive networks

supporting PWM reported in the behavioral literature (Spencer & Weber-Fox, 2014).

PT
3.4.4 Structural imaging findings in CWS

RI
In addition to functional imaging studies, a relatively small number of studies

SC
have also investigated structural differences between CWS and CWNS. Those studies

also implicate anomalies in regions considered to be important for attention/executive

U
function, sensorimotor integration, and PWM. Studies of gray matter volume (GMV)
N
have reported reduced GMV in the putamen and medial frontal gyrus (MFG), whereas
A
the right STG is reported to have higher GMV in CWS ages 9-12 years (Chang, Erikson,
M

Ambrose, Hasegawa-Johnson, & Ludlow, 2008) and CWS ages 6-12 years (Beal et al.,
D

2015). A comparison of recovered and persistent school-age CWS also showed more
TE

GMV the left and right STG in children who persist, suggesting that temporal lobe

auditory sensory regions play an important role in persistence and recovery (Chang et
EP

al., 2008). Studies of gray matter morphology in CWS have also reported differences in

the laterality of prefrontal regions in school-age children (8-13) (Mock et al., 2012) and
CC

the caudate nucleus of the BG (Foundas, Cindass, Mock, & Corey, 2013). In addition to

gray matter differences, weaker white matter connections (as measured by fractional
A

anisotropy; FA) between the left putamen and cortical networks associated with both

cognition and motor control (MFG, SMA, left IFG and insula) have also been observed

along with decreased connectivity between the left IFG and pSTG (Chang & Zhu, 2013;

40
Chang, Zhu, Choo, & Angstadt, 2015). Dorsal stream white matter connections,

including the left IFG and pSTG are also correlated with disassociations on a range of

neuromotor, articulatory, and receptive/expressive language measures, suggesting that

structural differences may underlie decreased neural efficiency for speech and

PT
language production (Choo, Burnham, Hicks & Chang, 2016). As such, structural

findings also implicate networks thought to support cognitive capacities underlying

RI
working memory emerging early in the development of stuttering (Zhu et al., 2013)

SC
3.4.5 Functional neuroimaging findings in AWS

U
While more than two decades of neuroimaging studies have shown widespread
N
functional and structural differences in AWS relative to TFS, findings have also been
A
inconsistent depending in part on the tasks used, sample sizes, neuroimaging approach
M

and analysis methodology (see Etchell et al., 2018 for comprehensive review; Ingham,
D

Grafton, Bothe, & Ingham, 2012; Neef, Anwander, & Friederici, 2015). Those caveats
TE

notwithstanding, there are several lines of evidence implicating differences in the

connections between the BG and sensorimotor networks involved in speech production.

EP

Neuroimaging studies have reported differences in the BG and along with premotor,

auditory, and cerebellar regions compared to TFS in the eyes-open resting state (Civier
CC

et al., 2013; Ingham et al., 2012; Ingham et al., 2004; Wu, Maguire, Riley, Fallon, &

LaCasse, 1995) during speech production tasks (Giraud, Neumann, & Bachoud-Levi,
A

2008; Ingham et al., 2012; Ingham et al., 2004; Watkins, Smith, Davis, & Howell, 2008;

Wu et al., 1995), and even during non-speech movements (Chang, Kenney, Loucks, &

Ludlow, 2009). Activity in the BG is also associated with measures of stuttering severity

41
and is related to the fluency enhancing effects of treatment (Giraud et al., 2008;

Toyomura, Fujii, & Kuriki, 2015). Taken together, those individual reports implicate BG

and sensorimotor networks in a range of conditions and suggest a relationship with

treatment effects.

PT
3.4.5.1 Evidence from meta-analyses

RI
In addition to individual reports, meta-analyses of positron emission tomography

SC
(PET) and fMRI udies also implicate structures within the BG with sensorimotor regions

involved in speech production (Belyk, Kraft, & Brown, 2015; Brown et al., 2005; Neef et

U
al., 2015). An early activation likelihood estimation meta-analysis across speech
N
production tasks found that AWS consistently present with increased activation in the
A
right IFG/insula and vermal region of the cerebellum, with decreased activation in the
M

bilateral STG during speech production (Brown et al., 2005). Those findings were
D

interpreted as an error in the process of internal model formulation in which suppression

TE

of the auditory areas below baseline (i.e., inhibitory forward models) causes an error

signal to be sent back to motor areas that, in turn, causes a predict-correct loop (e.g.,
EP

part-word repetitions) (Brown et al., 2005). Two more recent functional imaging meta-

analyses also reported patterns of activity related to trait (i.e., TFS compared to AWS)
CC

and state (i.e., disfluent speech relative to fluent speech) aspects of stuttering (Belyk et

al., 2015; Budde, Barron, & Fox, 2014). In trait analyses, right-hemisphere over
A

activations include the PMC, primary motor-cortex, rolandic operculum, insula, posterior

IFG, orbital IFG, pre-SMA, MFG, IPL, and SPL. Left-hemisphere under activations

include laryngeal motor cortex, MTG, STS, vermal region of the cerebellum, and red

42
nucleus of the midbrain, suggesting widespread neurocognitive networks are involved in

stuttering by adulthood. By contrast, state analyses comparing disfluent and fluent

speech have found areas related to disfluency are primarily in the left-hemisphere (e.g,

IFG, SMA, somatosensory cortex, and BG), while areas related to fluency are found in

PT
right-hemisphere regions (primary auditory cortex (A1), PT, pSTG, SMG, IPL, & IFG). In

those meta analyses, the only fluency related region in the left was the SMG,

RI
suggesting that left somatosensory association areas may also play a role in fluency or

SC
compensation for sensorimotor instabilities in the audio-motor network (Belk et al.,

2015; Budde et al., 2014; Neef et al., 2015). Taken together, state analyses suggest

U
that regions consistent with typically left-hemisphere dominant frontotemporal-parietal

N
network are under-active in AWS during stuttered speech. On the other hand, fluency
A
related areas in the right hemisphere are hyperactive during fluent speech, suggesting
M

that right-hemisphere structures may aid in compensation for sensorimotor instabilities

on the left. Those findings are consistent with differences in dorsal stream regions
D

proposed to mediate the emergent properties of PWM and sensorimotor integration in

TE

speech production.
EP

3.4.5.2 Evidence from resting-state networks

CC

Another line of evidence implicating broader neurocognitive networks in DS is

recent evidence from the resting state. One distinct weakness of functional
A

neuroimaging studies employing various speaking and reading tasks is that it is difficult

to compare activations across studies due to task differences (Chang et al., 2017;

Etchell et al., 2018). While early findings suggested a lack of consistent differences in

43
the resting-state, more recent studies using larger sample sizes and more recent

analytic approaches have noted differences (Etchell et al., 2018). Xuan and colleagues

(2012) reported that networks associated with cognitive control including increased

connectivity in the prefrontal cortex and DMN and increased connectivity in motor and

PT
auditory regions. Lu and colleagues (2012) reported decreases in functional connectivity

during resting state in the left IFG and dorsolateral prefrontal cortex compared to TFS.

RI
In that study, AWS who received treatment showed reduction in the left IFG and

SC
increases in the SMA and cerebellum, suggesting that treatment effects may have been

related to compensatory speech timing networks. Yang, Fanlu, Siok, and Tan (2016)

U
also reported reduced resting-state connectivity between the right SMA and BG, along

N
with decreased connectivity between the STG and BG. More recent studies have also
A
found differences in resting state connectivity between the left IFG and primary auditory
M

cortex/Heschl's gyrus that is correlated with performance on a speech perception task,

further suggesting a relationship between intrinsic differences in sensorimotor networks

D

and challenging speech processing tasks (Halag-Milo et al., 2016; Lu, Long, Zheng, Shi,
TE

& Liu, 2016). Thus, resting state findings imply differences in large-scale neurocognitive
EP

networks in AWS, including aspects of the PFC, BG, and regions involved in dorsal

stream sensorimotor integration in speech production and challenging speech

CC

perception tasks.
A

3.4.5.3 Evidence for the PFC in compensation and unassisted recovery

While resting state findings implicate attention and executive function in AWS,

they do not explicitly link it to moment-to-moment variability in stutter-typical disfluencies

44
during speech production. However, recent functional neuroimaging findings in AWS do

implicate the left and right orbitofrontal cortex (OFC) in compensation for stuttering

(Sitek et al., 2016) and in unassisted recovery from stuttering in adulthood (Kell et al.,

2017). Using resting state and diffusion MRI, Sitek and colleagues (2016) reported that

PT
AWS with the least severe symptoms as determined by the Stuttering Severity

Instrument – Fourth Edition (SSI-4; Riley, 2009) presented with increased functional and

RI
structural connectivity between the OFC and cerebellum compared to AWS with higher

SC
SSI-4 severity ratings, suggesting that the OFC/cerebellum could be involved in

compensatory mechanisms in the more fluent AWS. Further, long-lasting recovery

U
without treatment (i.e., recovered stuttering) in AWS has been associated with

N
differences in the left ventrolateral prefrontal cortex (orbital IFG; BA47/12) (Kell et al.,
A
2009). More recent functional connectivity analyses have reported ‘hyperconnectivity’
M

between BA47, BA44, the SMA, and SMG prior to fluency shaping therapy. Following

therapy, reductions in connectivity were observed between BA44 (i.e., opercular IFG)
D

and the SMG along with increased coupling between the anterior STG and ventral
TE

motor cortex. By contrast, in recovered stuttering, there was decreased connectivity

EP

from BA47 to the SMA, SMG, and superior cerebellum, suggesting that the OFC

modulates somatomotor connectivity in recovered stuttering differently than in treated

CC

AWS. Thus, recent evidence implicates the PFC in both enhancing fluency and

potentially in increasing stutter-typical disfluencies, similar to dual-task findings that load

A

aspects of attention and executive function.

3.4.6 Structural findings in AWS

45
 Evidence from recent structural neuroimaging studies comparing AWS and TFS

implicates connectivity between PFC, BG, and dorsal stream regions. One line of

evidence in particular implicates structural differences in the PT with at least some AWS

demonstrating greater overall area and a more symmetric pattern in the PT (Foundas,

PT
Bollich, Corey, & Hurley, 2001). Enhanced fluency induced by delayed auditory

feedback in a subgroup of AWS is also associated with rightward PT asymmetry

RI
(Foundas, Bollich, Feldman, & Corey, 2004). Other studies have reported increased

SC
white matter underlying the right PT, further suggesting that compensatory processing

in the right PT may be related to white matter plasticity and compensation for anomalies

U
in the left PT (Jäncke, Hänggi, & Steinmetz, 2004). Despite these early findings, the role

N
of PT asymmetry in DS is uncertain, as later studies with larger sample sizes and more
A
stringent controls (e.g., inclusion of only right-handed adults) have not replicated gray
M

matter PT asymmetry in AWS relative to TFS (Chang et al., 2008; Cykowski et al.,

2008; Gough et al., 2018). One possible mediating factor is variability in the age of
D

study participants. For example, Gough and colleagues (2018) reported a positive
TE

correlation between PT asymmetry and age in TFS while no such relationship was
EP

observed for AWS. Another possibility is that there are subtypes of AWS in whom PT

asymmetry interacts with structural or functional anomalies in other cortical or

CC

subcortical structures (Foundas, et al., 2013; Gough et al., 2018). Those uncertainties

notwithstanding, PT asymmetry or PT connectivity with other dorsal stream structures

A

implicates structural differences in region thought to be critical for audiomotor

integration and PWM in the dual-stream model.

46
 A second line of evidence supporting dorsal stream pathophysiology comes from

structural differences in regions thought to be connected to the PT. Decreases in gray

matter volume of AWS have also been reported in other structures consistent with PWM

buffers thought to be important for articulatory rehearsal. These areas include the IFG

PT
and aspects of the more anterior STG (Beal, Gracco, Lafaille, & Luc, 2007; Song, Peng,

Jin, Yao, & Ning, 2007). In particular, decreased gray matter volume in the left IFG has

RI
been found to negatively correlate with stuttering severity (Kell et al., 2009). Recent

SC
findings also suggest that the right BG and bilateral STG functionally and structurally

are more strongly connected than in TFS (Sitek et al., 2016). Sowman and colleagues

U
(2017) have also reported differences in gray matter volume of the caudate nucleus in

N
AWS, while a number earlier studies reported differences in the right precentral gyrus
A
and STG (Beal et al., 2007; Kikuchi et al., 2011; Song et al., 2007). In addition to gray
M

matter anomalies, studies have also reported white matter differences in areas

important for connecting premotor structures with somatosensory and audio-motor

D

regions (Cai et al., 2014). Further, anomalies along white matter tracts connecting
TE

dorsal stream regions may also be present in the peripheral nervous system along the
EP

corticobulbar and corticospinal tracts, suggesting that dorsal stream anomalies may be

related to decreased efficiency of peripheral execution (Connally, Ward, Howell, &

CC

Watkins, 2013). A recent ALE meta-analysis in AWS also reported decreased FA in

white matter tracts connecting left hemisphere frontal motor structures (IFG, vPMC,
A

primary motor cortex) with temporal structures (pSTG, middle temporal gyrus; MTG)

and parietal structures (SMG, primary somatosensory cortex) (Neef et al., 2015).

47
 While methodological limitations make attributing white matter anomalies to the

dorsal stream as opposed to the ventral stream uncertain, recent studies have reported

a lack of white matter differences in the ventral stream with robust differences in the

dorsal stream (see Kronfeld-Duenias, Amir, & Ezrati-Vinacour, 2017 for debate). Finally,

PT
in the most recent study implicating the PFC in stuttering, Neef and colleagues (2017)

reported that increased connection strength between the right frontal pole (BA10) and

RI
subthalamic nuclei is positively correlated with stuttering severity, while the uncinate

SC
fasciculus connecting the right frontal pole to auditory and multisensory regions was

negatively correlated with stuttering severity, suggesting that aspects of the frontal pole

U
may be related both to compensatory and inhibitory processes affecting fluent speech

N
production. Taken as a whole, the structural imaging literature suggests anomalous
A
connectivity in large-scale neurocognitive networks including the PFC, BG, and dorsal
M

sensorimotor stream implicated in PWM, while differences in the ventral stream

important for lexical access remain uncertain.

D
TE

3.4.7 Implications of neuroimaging findings in CWS and AWS

EP

Although a number of interpretations have been proposed to account for

neuroimaging findings in CWS and AWS, a common theme is that both CWS and AWS
CC

present with differences in networks thought to mediate timing in speech-motor control

and sensorimotor integration. Despite considerable spatial variability across studies, in

A

a systematic review of the neuroimaging literature, Etchell et al. (2018) concluded that

one common finding in both CWS and AWS is decreased activation and reduced gray

matter volume in the left IFG and connections with the SMA, temporal lobe regions, and

48
right IFG. Additionally, in the only study to examine anomalous structure and function in

CWS and AWS, the IFG (pars opercularis) was also reported to be the only region to

show an abnormal developmental trajectory (reduced gray matter thinning), suggesting

that gray matter anomalies or underlying white matter anomalies are a strong candidate

PT
for the cause of anomalous input to the sensorimotor network in the preschool years

(Beal et al., 2015). Interestingly, the triangular and opercular portions of the IFG are

RI
also causally related to the transmission of information for timing and sequencing in

SC
speech production as opposed to articulatory quality located in more dorsal premotor

regions (Long, Katlowitz, Svirsky, & Clary, 2016). The commonly reported hyperactivity

U
in the right IFG (Belyk et al., 2015; Brown et al., 2005; Budde et al., 2014), thought to

N
compensate for deficits in the left IFG, is also considered a core structure active across
A
a range of conditions requiring the processing of temporal information in perception and
M

motor control (Weiner, Turkeltaub, & Coslett, 2010). As such, neuroimaging findings

suggest that differences in the efficiency of timing networks related to both dorsal
D

stream sensorimotor integration and the emergent properties of PWM are different in
TE

both CWS and AWS. In this way, the available neuroimaging literature suggests that
EP

behavioral differences in accuracy on tasks heavily recruiting those same networks,

such as nonword repetition or dual-tasks, are likely in both CWS and AWS.
CC

Finally, in CWS regions within the PFC appear to be related to persistence and

recovery in connection with sensorimotor networks (Chang et al., 2017). In AWS,

A

subregions of the PFC in connection with sensorimotor networks also appear to be

related to compensation for stuttering (Sitek et al., 2016), treatment effects (Kell et al.,

2009), and unassisted recovery (Kell et al., 2017). The most recent study to date to

49
interpret functions of the PFC also suggested that different right hemisphere

connections may subserve both fluency enhancing compensatory and detrimental

inhibitory processes, suggesting that the right PFC via different pathways may be

involved in processes that are both deleterious to and facilitate fluency in AWS (Neef et

PT
al., 2017). Those findings are broadly consistent with discrepant dual-task effects on

stuttering depending on the experimental conditions (Bosshardt, 2006). Taken together,

RI
those findings are consistent with a modulatory role for the PFC that may be related to

SC
both compensation for sensorimotor instabilities and conditions that increase the

likelihood of stuttering.

U
4. Linking brain and behavior N
A
Differences in connectivity of the PFC, BG, and dorsal stream sensorimotor
M

regions may provide explanations for common behavioral findings in nonword repetition,
D

auditory-perceptual, and dual-tasks in DS. First, disrupted timing cues from the forward
TE

model to the inverse model affecting speech production could explain subtle behavioral

differences commonly observed on nonword repetition tasks in preschool CWS

EP

(Spencer & Weber-Fox, 2014). If differences in sensorimotor timing or ‘high variance’

input to internal models of motor control account for incorrect nonword repetition trials,
CC

the process would not always be expected to result an incorrect response. In other

words, on some trials CWS would be expected to compensate for increased variance or
A

interbuffer timing differences much like they would in natural speech production (i.e.,

perceptually fluent speech) (c.f. Namasyam & van Lieshout, 2011). Such a mechanism

might account for statistically significant differences in nonword repetition that are

50
 nonetheless within normal limits in preschool CWS (Pelczarski & Yaruss, 2016). In

AWS, the proposal is consistent with differences in fine motor control during nonword

repetition tasks at lower loads (e.g., 4 syllables), suggesting compensation for

sensorimotor instabilities (Smith et al., 2010; Smith et al., 2012), while behavioral

PT
differences emerge only when the PWM system is heavily loaded (Byrd et al., 2012;

Byrd et al., 2015; Coalson & Byrd, 2017). Finally, while lower performance on nonword

RI
repetition tasks is commonly observed in CWS, semantic repetition tasks typically do

SC
not result in significantly lower accuracy (Spencer & Weber-Fox, 2014; Anderson &

Wagovich, 2010; Pelczarski & Yaruss, 2016) and do not appear to be related to

U
persistence and recovery (Spencer & Weber-Fox, 2014). Interestingly, syntactic phrase

N
structure violations embedded in sentences with semantic content are not associated
A
with processing differences between CWS who recover and those who persist, but
M

similar violations are associated with processing differences (i.e., N400-like response)

between the two groups in nonsense ‘jabberwocky’ phrase repetition tasks. Those
D

findings suggest limitations on PWM interacting with syntax may also related to
TE

persistence/recovery while semantic processes alone are not (Usler & Weber-Fox,
EP

2015). Taken together, findings are more consistent with dorsal stream pathophysiology

than ventral stream pathophysiology proposed to mediate LTM for semantic content or
CC

lexical access (Hickok et al., 2011; and see Majerus, 2013) and may explain why single

word, verbal repetition tasks typically do not result in significantly lower behavioral
A

performance or predict persistence/recovery.

Second, a deficit in dorsal stream sensorimotor integration is consistent with lines of

evidence suggesting neurobiological and subtle behavioral differences between PWS

51
and controls in challenging auditory perception tasks in the absence of a functional

deficit in language comprehension (Chang, et al., 2009; Dailiri & Max, 2015; Halag-Milo

et al., 2016; Neef et al., 2012; Saltuklaroglu et al., 2017; Sato, Mori, Koizumi, &

Minagawa-Kawai, 2011). According to the dual-stream model, the dorsal stream may

PT
aid perceptual tasks in which working memory and attention are focused on speech-

sound analysis, whereas the ventral stream mediates receptive processing wherein the

RI
goal is linguistic comprehension (i.e., a double dissociation) (Hickok & Poeppel, 2007).

SC
Forward models of speech production may be adapted in some instances to difficult

perceptual tasks (e.g., discrimination in noise), allowing for constraints on expected

U
upcoming speech percepts that may later aid working memory for the subsequent

N
response (e.g., via covert rehearsal) (Hickok et al., 2011). Thus, mistimed or ‘noisy’
A
sensorimotor integration would be expected to cause subtle differences in auditory-
M

perceptual tasks without functional language comprehension deficits. Given the link

between sensorimotor integration in speech perception and production, PWM may also
D

be related to a higher risk of phonological disorders in children who stutter (Ambrose,

TE

Yairi, Loucks, Seery, & Throneburg, 2015). As such, the evidence implicates
EP

differences in the dorsal sensorimotor network that are related to auditory speech

processing, phonological storage, and the sensorimotor control of speech production in

CC

the absence of functional language comprehension deficits thought to be mediated by

the ventral stream.

A

Third, there is some evidence from preschool-age CWS that aspects of attention

interact with the process of phonological storage for nonword repetition (Anderson &

Wagovich, 2010) and the neurocognitive networks supporting attention and executive

52
function are implicated in persistence and recovery (Chang et al., 2017). A potential role

for the PFC and BG in executive control of both working memory under distracting

conditions and speech production under attentionally demanding conditions (e.g., social

situations or under time-pressure) is consistent with those findings and recent brain

PT
imaging evidence implicating both intrinsic and disfluency related neurocognitive

networks in CWS and AWS (Chang et al., 2017; Kell et al., 2017; Sitek et al., 2016). In

RI
such case, tasks that ensure attention is directed away from speech production,

SC
decoupling of the PFC-BG and dorsal sensorimotor/cerebellar network would be

expected along with fluency enhancement (e.g., Eichorn et al., 2017; Vasic & Winjin,

U
2005). However, in other tasks in which attention is directed internally to speech

N
production (e.g., Bosshart, 2002; Caruso & Chodzko-Zajko, 1994) or that load highly
A
overlapping cognitive-linguistic processes (Bosshardt, 2002; Metten et al., 2011),
M

greater PFC-BG coupling with the dorsal stream would be expected along with

instabilities in dorsal stream sensorimotor timing. That potential function of PFC-BG

D

modulation of the dorsal stream during internal model formulation is broadly consistent
TE

with the OFCs role in compensation for sensorimotor instabilities and disconnection of
EP

the OFC from the audiomotor and somatosensory regions in unassisted recovery (Kell

et al., 2017). Thus, the PFC may be important in compensating for internal sensorimotor
CC

errors in addition to increasing the probability of stuttering depending upon the

circumstances. To investigate those possibilities, future work would need to carefully

A

manipulate the direction of attention in dual-tasks and the extent to which cognitive

resources are shared between tasks.

53
5. Future directions: Neural oscillations in PWM

While there appear to be links between the neurobiology of stuttering and PWM,

it is still unclear what precise mechanisms mediate that relationship. We suggest that

mechanisms underlying differences in sensorimotor control and PWM in CWS and AWS

PT
could be further explored by investigating cyclic dorsal stream interbuffer timing

differences in nonword repetition and dual-tasks guided by the neurobiological networks

RI
reviewed. Figure 1 depicts cortical networks likely to be related to PWM according to the

SC
dual-stream model proposed by Hickok and Poeppel (2007) (blue, green, yellow) and

more recent models and data proposing an executive network involved in attentional

U
control (red) (D’Esposito, 2007; Majerus, 2013; Nee et al., 2013). While it is difficult to
N
examine cyclic interbuffer timing in the encoding, maintenance, and production phases
A
of a nonword repetition task when using relatively low temporal resolution imaging
M

approaches (e.g., fMRI), one way to investigate ongoing sensorimotor timing in each
D

phase of the task is via event-related changes in the ongoing time-frequency of the

electroencephalography (EEG) and magnetoencephalography (MEG) known as ‘neural

TE

oscillations.’ According to a ‘dynamic’ model of oscillatory function, neural oscillations

EP

are critical for long-distance interregional communication and timely correlations

between the phase of oscillations in prefrontal regions and sensorimotor regions may
CC

reflect top-down control of interregional communication in both perception and action-

control. (Fries, 2005; Siegel, Donner, & Engel, 2012). As such, the power and phase of
A

neuronal oscillations has the potential to allow for the study of large scale neuronal

dynamics in the various stages of nonword repetition related to stimulus encoding, trace

maintenance, and repetition (i.e., execution).

54
 Multifactorial models of stuttering have long predicted that even subtle

differences in cognitive capacities affect motor control for speech in DS (Smith, 1999;

Starkweather, 2002). In particular, the speech motor skill (SMS) framework predicts that

cognitive-sensorimotor loads may destabilize central neural oscillators, resulting in

PT
decreased oscillatory entrainment with speech-motor effectors critical for feedback

control (Namasivayam & van Lieshout, 2011; van Lieshout, Ben-David, & Lipski, 2014;

RI
van Lieshout et al., 2004). From that point of view, the repetition of novel phonological

SC
sequences and dual-tasks loading cognitive-sensorimotor oscillators may cause load-

dependent breakdowns in entrained sensorimotor-effector oscillations. One likely

U
difference related to sensorimotor timing in AWS and CWS is neural oscillations in the

N
beta band (15-25Hz) (Etchell et al., 2014). The beta band is a known correlate of motor
A
activation and more recently has been proposed to mediate coordinative timing in
M

audio-motor integration for speech along with lower frequency bands (Morillion &

Schroeder, 2015). In CWS differences in the beta band have been found at rest (Özge,
D

Torosm & Çömelekoğlu, 2004) and reversals in the timing of peak beta band power
TE

reduction (i.e., suppression) and enhancement in a rhythmic tone perception task has
EP

been observed in CWS relative to CWNS (Etchell, Ryan, Martin, & Johnson, 2016). In

AWS, differences have been found beta band interhemispheric connectivity at rest
CC

(Joos, De Ridder, Boey, & Vanneste, 2014), in speech production tasks (Mersov,

Cheyne, Jobst, & De Nil, 2017), and in speech perception tasks (Saltuklaroglu et al.,
A

2017). As such, we suggest that the study of neural oscillations in nonword repetition

and dual-tasks may provide a means of investigating a much needed link between the

sensorimotor mechanisms proposed to mediate stutter-typical disfluencies (Hickock et

55
al., 2011; Tian & Poeppel, 2012) and sensorimotor mechanisms mediating PWM

(Herman et al., 2013). Finally, if underlying dorsal stream timing mechanisms can be

identified in oscillatory bands, such methods may inform frequency specific approaches

to neurofeedback or neuromodulation such as transcranial alternating current

PT
stimulation (Ali, Sellers, & Frohlich, 2013) in tasks designed to manipulate

attention/executive function and working memory (e.g., see Metten et al., 2011). In this

RI
way, the study of the relationship between cognitive-load and sensorimotor oscillations

SC
may lead to more specific neuromodulatory targets to augment current behavioral

treatment approaches.

U
6. Conclusions and cautions N
A
The primary aim of the current review was to further explicate how the
M

neurobiological networks implicated in stuttering could be related to reported differences

D

in nonword repetition and dual-task performance. To that end, we highlighted a number

TE

of findings from nonword repetition and dual-task paradigms that are broadly consistent

with a role for sensorimotor and executive capacities underlying PWM. Second, we
EP

proposed that current neurobiological models of language, executive function, and

neuroimaging findings in DS are consistent with overall lower capacities on tasks that
CC

place a heavy load on PWM and sensorimotor integration. Taken as a whole, there is

accumulating evidence that the emergent properties of PWM are related to the dorsal
A

stream and are modulated by PFC-BG connectivity both of which have been strongly

implicated in the pathophysiology and behavior of DS (Etchell et al., 2018). Because

behavioral tasks thought to load those same networks may be related to the

56
subtypes/phenotypes of recovery and persistence in CWS (Spencer & Weber-Fox,

2014) and unassisted recovery in adulthood (Kell et al., 2017), we believe that attempts

to bridge the gap between cognitive-behavioral and brain findings may result in further

insights into the cognitive operations underlying those important phenomena.

PT
While the review suggests parallels between the capacities mediated by PWM

and the neurobiological networks supporting them, some caution is also warranted.

RI
First, although we hypothesize that cyclic timing errors in sensorimotor mapping will be

SC
related to load-dependent processing in CWS and AWS (e.g. in a nonword repetition

task), it is unclear how errors in sensorimotor mapping lead to overt, stutter-typical

U
disfluencies in more naturalistic communicative interactions. The difference in

N
sensorimotor integration for speech production proposed to account for stuttering and
A
here to mediate lower PWM capacity is also considered subtle and highly load-
M

dependent. Further, organization for language appears to share features with other

cognitive domains, potentially allowing for multiple interactions between linguistic and
D

other cognitive processes in naturalistic speaking contexts (Frederici & Singer, 2015).
TE

Overt stuttered moments, as opposed to sensorimotor errors in timing, may also be an

EP

emergent process requiring multiple, dynamic interactions between cognitive-linguistic,

cognitive-emotional, and sensorimotor processes (Namasivayam & van Lieshout, 2011;

CC

Smith, 1999; Smith & Weber, 2017; Starkweather, 2002; van Lieshout et al., 2004). In

other areas of neuroscience, significant advances in understanding the relationship

A

between brain and behavior have relied on similar concepts of multiple realizability

driven by previous theoretical and experimental decomposition of behavior (Krakauer,

Ghazanfar, Gomez-Marin, MacIverr, & Poeppel, 2017). As such, to understand the

57
relationship between stuttering and cognitive-sensorimotor capacities, future work will

need to examine the relationship between internal errors in sensorimotor mapping,

carefully defined behavioral measures of cognitive-sensorimotor load, and the pathway

by which multiple interactions between those processes lead to what listeners perceive

PT
as overtly stuttered moments.

Another note of caution is that the neurobiological models discussed in this

RI
review are themselves the subject of ongoing controversy, including ongoing discussion

SC
about the functional segregation of the PT region in speech processing (Hickok &

Poeppel, 2007). There is also evidence that the dorsal stream is more bilaterally

U
organized than the dual-stream model indicates, with different functions in the right and

N
left hemispheres (Ylinen et al., 2014). Similarly, controversies concerning the functional
A
role of various prefrontal regions in executive function and attentional control are also
M

ongoing and it is likely that different PFC regions (e.g. medial vs. lateral) have different

functional roles (Koechlin & Summerfield, 2007). Finally, neuroimaging findings in PWS
D

vary considerably across studies (Etchell et al., 2018; Ingham et al., 2012; Neef et al.,
TE

2015) and structural imaging methodology is currently limited. For those reasons,
EP

differences in particular regions or tracts should be interpreted cautiously (Etchell et al.,

2018). Finally, neural networks that are stable within an individual AWS nonetheless
CC

differ significantly between AWS, suggesting significant interindividual differences in

neural networks depending on previous experiences with stuttering (Wymbs, Ingham,

A

Ingham, & Paolini, 2013). Such a finding is not surprising considering that individual

PWS have variable phenomenological experiences (Plexico, Manning, & DiLollo, 2005)

58
and to some extent functional reorganization would be expected to reflect those

experiences (Ingham et al., 2012; Wymbs et al., 2013).

Despite the above cautions, further investigation of the link between the

neurobiological underpinnings of PWM and stuttering has a number of advantages.

PT
First, the study of PWM has the advantage of a rich theoretical history, stable and

replicable empirical paradigms, and supporting neurobiological networks that have also

RI
been implicated in both CWS and AWS. Second, because much of the neuroimaging

SC
literature in stuttering has not been driven by current neurobiological models of

language and cognition, the application of models outside the field could potentially

U
facilitate collaboration across laboratories. Finally, if PWM is related to variability in the

N
expression of stuttering, it may aid in explaining interindividual differences in brain
A
networks. The networks implicated here predict the extent to which relevant information
M

is stored and are associated with individual differences in working memory capacity

(McNab & Klingberg, 2008). As such, a better understanding of the mechanisms

D

underlying PWM has the potential to explain how sensorimotor loads or capacities are
TE

related to individual differences in brain networks. In the future, investigations may

EP

continue to aid in identifying CWS who are more likely to persist or recover and AWS

that would benefit from cognitive-behavioral or mindfulness training approaches

CC

focusing on cognitive-linguistic and cognitive-emotional processes (Boyle, 2011;

Menzies, Onslow, Packman, & O’Brian, 2009).

A

59
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 Bio Notes

Andrew Bowers, Ph.D. CCC-SLP is an Assistant Professor at the University of

Arkansas where he directs the EEG Neurofeedback Laboratory. He conducts research
focusing on sensorimotor integration in speech perception and production using high
density electroencephalography (EEG), autonomic measures, and surface

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electromyography (EMG). His research examines relationships between sensorimotor
integration, cognition, and measures of task-performance toward non-invasive brain-
computer interface methods designed to augment treatment approaches in fluency

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disorders.

Lisa Bowers Ph.D. CCC-SLP is an Assistant Professor at the University of Arkansas.

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Her research focuses on the speech, language, and literacy abilities of children from
infancy to adolescence. She is a certified speech-language pathologist and has
experience in Early Intervention and school settings working with children from culturally
and linguistically diverse backgrounds.

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Dan Hudock, Ph.D., CCC-SLP, is an Associate Professor in Communication Sciences
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and Disorders at Idaho State University and Director of the Northwest Center for
Fluency Disorders. His research interests are psycho-social-emotional aspects of
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fluency disorders, interprofessional collaborations with mental health professionals for
the holistic assessment and treatment of fluency disorders, and the neuroscience of
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speech perception and production in people who stutter using high-density

electroencephalography (EEG) time-course analysis.
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Heather L. Ramsdell-Hudock, PhD CCC-SLP, University of Memphis, 2009, is an

Associate Professor at Idaho State University. She leads the Infant Vocal Development
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Laboratory and her research and teaching interests span infant vocal development,
caregiver-infant reciprocity, phonetics, phonology, the scholarship of teaching and
learning, and mentoring graduate and undergraduate students through the scientific
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process.
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Figure 1. A depiction of networks likely to interact in nonword repetition and dual-

tasks based on Hickok and Poeppel’s dual-stream model (Hickok and Poeppel,
2007) (blue, green, yellow) and an attentional/executive network in working
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memory (see Majerus et al., 2013 and Nee et al., 2013) (red). Regions in red include
the dorsolateral prefrontal cortex (DLPFC), the ventrolateral prefrontal cortex (VLPFC),
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inferior parietal lobule (IPL) and superior parietal lobule (SPL). The dorsal stream
includes the IFG, PMC, and PT/Spt regions (blue) along with the primary auditory cortex
(green) and superior temporal sulcus (yellow).
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 Appendix A.

Table A.1 Summary of nonword repetition studies in preschool-age children who stutter.

Study Age (range) N Matching Difference in nonword Maximum Difference Effect Size

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repetition accuracy syllable in kinematic
length measures
Hakim & Ratner (2004) 4;1-8;4 8 CWS; 8 CWNS age, sex, maternal education yes 5 NM d=1.41

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Anderson et al. (2006) 3;0-5;2 12 CWS; 12 CWNS age, sex, SES yes 5 NM 𝜂2 =.29
Anderson & Wagavich (2010) 3;6-5;2 9 CWS; 14 CWNS none yes 5 NM 𝜂2 =.42
Smith et al. (2012) 4-6 31 CWS; 22 CWNS SES no* 4 yes NR

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Spencer & Weber-Fox (2014) 3;9-5;8 21 CWS-Rec; 9 CWS-Per; age, SES, nonverbal reasoning yes 4 NM NR
25 CWNS
Pelczarski & Yaruss (2016) 5;5-5;8 11 CWS; 11 CWNS age, language ability, sex, maternal yes 7 NM NR

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Note. CWS = children who stutter; CWNS = children who do not stutter; CWS-Rec = children who stutter, recovered; CWS=Per = children who stutter who persist; SES= Socioeconomic Status; NM = not
measured; NR = not reported
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*Smith et al., (2012) did not report significant differences in overall accuracy of nonword repetition between CWS and CWNS groups, but did report a significant difference for CWS with articulation/language
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disorders.
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Table A.2 Summary of nonword repetition studies in school-age children who stutter.
 Study Age (range) N Matching Difference in nonword Maximum Difference in Effect Size
repetition accuracy syllable kinematic
length measures
Seery et al. (2006) 8;6-12;6 14 CWS; 11 CWNS none yes* 5 NM NR
Bakhtiar et al. (2007) 5;1-7;10 12 CWS;12 CWNS none no 3 NM NR
Chon & Ambrose (2007) 10-13 14 CWS-Rec;5 CWS-Per none no 4 NM NR
Weber-Fox et al. (2008) 9;4-13;9 10 CWS; 10 CWNS age, sex no** 3 NM NR

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Oyoun et al. (2010) 5-13 30 CWS; 30 CWS age,sex yes*** 3 NM NR
Sasisekaran & Byrd (2013) 8-15 14 CWS;14 CWNS age, sex no**** 4 NM NR

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Note. CWS = children who stutter; CWNS = children who do not stutter; CWS-Rec = children who stutter, recovered; CWS=Per = children who stutter who persist; NM = not measured; NR = not reported

*Seery et al., (2006) reported a significant interaction between group and syllable length and reported significant differences in post-hoc comparisons between CWS and CWNS at 5-syllable length

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**Weber et al. (2008) reported similar nonword repetition accuracy in both groups that was comparable to 30 CWNS in the same age range in a previous study.

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***Oyoun et al. (2010) also reported a significant correlation between subject age and severity with nonword repetition performance.

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****Sasisekaran & Byrd (2013) further subdivided CWS into younger (7-11) and older groups (11-15) and reported significant differences in a phoneme elision task between younger and older groups and no
differences between age matched CWNS groups.
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Table A.3 Summary of nonword repetition studies in adults who stutter.

Study N Matching Difference in nonword Maximum Difference Effect Size

repetition accuracy syllable length in kinematic
measures
Ludlow et al. (1997) 5 AWS; 7 TFS none yes 4 NM NR
Namasiyam & van Lieshout (2008) 5 AWS; 5 TFS age, sex, education level NM 4* yes d=1.64
Smith et al. (2010) 17 AWS; 17 TFS age, sex, education level no 4 yes NR

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Byrd et al. (2012) 14 AWS; 14 TFS age, sex yes 7** NM 𝜂 =.15
Sasisekaran (2013) 9 AWS; 9 TFS age,sex no 4*** yes 𝜂2 =.32
Sasisekaran & Weisberg (2014) 10 AWS; 10 TFS age, sex yes 6 yes NR

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Byrd et al. (2015) 10 AWS; 10 TFS age, sex, education level yes 7 NM 𝜂 =.38
Coalson & Byrd (2017) 26 AWS; 26 TFS none yes 2**** NM d=.34

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Note. AWS = adults who stutter; TFS = typical fluent speakers; NM = not measured; NR = not reported

*Namasiyam & van Lieshout (2008) reported practice effects on two bisyllable, bilabial nonword productions. The effect size reported is for a main effect of movement amplitude.

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**Byrd et al., (2012) reported a significant interaction between group and syllable length in a nonword condition with 7 syllables.
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***Sasisekaran (2013) reported no differences on a nonword repetition task but did reported differences on kinematic measures during a nonword reading task. The effect size reported is for lip aperture variability
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****Coalson & Byrd (2017) used only two syllable lengths but manipulated stress patterns and reported a significant interaction of talker group, stress, and task indicating that group differences were driven by
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only the most demanding conditions (e.g., low frequency stress patterns)
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Table A.4 Summary of dual-task studies in adults who stutter.

Study N Matching Differences in primary Differences in secondary Effects on stuttering

task/measures task/measures
Caruso et al. (1994) 9 AWS; 9 TFS none yes (latency, speech rate) no (Stroop color word) increases
Bosshardt et al. (1999) 9 AWS;10 TFS mental calculation performance yes (inhalation rate, length of no (mental calculation) increases primarily in a
breath group, word duration) subgroup of AWS
De Nil & Bosshardt (2000) 12 AWS;12 TFS none *(sentence planning) * NR (rhyme and category *NM
decisions)

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Bosshardt et al. (2002) 14 AWS; 16 TFS age, education, sex, memory span, no (pause rate, inhalation rate) **yes (reading and memorizing increases
vocabulary phonologically similar and
dissimilar words)

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Bosshardt et al. (2002) 14 AWS;16 TFS age, education, sex, digit span, ***yes (# of propositions in no (rhyme and category decisions) no change
vocabulary sentence production)
Vasic & Wijnen (2005) 22 AWS;10 TFS none no (narrative retell) ****NM decreases

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Smits-Bandstra & De Nil (2009) NM
Jones et al. (2012) 9 AWS; 9 TFS sex, educational background no (rhyme judgement) yes (letter recall) NM
Maxfield (2016) 15 AWS; 15 TFS none yes (naming accuracy) no (tone judgement accuracy) NM
Eichorn et al. (2016) 20 AWS; 20 TFS none *****no (speech errors) no (spatial working memory and decreases

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digit span tasks)
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Note. AWS = adults who stutter; TFS = typical fluent speakers; NM = not measured; NR = not reported
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*De Nil & Bosshardt (2000) used a sentence planning task wherein no behavioral measures were available. No measures of language production, stuttering, or statistical tests of rhyming and category
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decisions were reported.

**Bosshardt et al. (2002) reported significantly lower word recall accuracy in the TFS group compared to the AWS group.
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***Bosshardt et al. (2002) reported significantly a higher percentage of stuttered syllables in the AWS group relative to controls but dual-tasks were not associated with more stuttering than sentence
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production.

****Vasic & Wijnen (2005) used a distracting video game in simple and more challenging conditions but did not report behavioral performance on the task.
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*****Eichorn et al. (2016) did not report more speech errors in dual-tasks conditions for AWS relative to controls but did report lower speech rate in the AWS group compared to controls.
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