You are on page 1of 12

Effects of Early Auditory Deprivation on Working

Memory and Reasoning Abilities in Verbal and


Visuospatial Domains for Pediatric Cochlear Implant
Recipients
Lisa S. Davidson,1 Ann E. Geers,2 Sandra Hale,3 Mitchell M. Sommers,3 Christine Brenner,4
and Brent Spehar1

Objectives: The overall goal of this study was to compare verbal and visuo- processing including sensation, perception, attention, learning,
spatial working memory in children with normal hearing (NH) and with and memory. This type of model views the human nervous sys-
cochlear implants (CI). The main questions addressed by this study were tem as an information-processing system that encodes, stores,
(1) Does auditory deprivation result in global or domain-specific deficits in and manipulates various types of symbolic representations
working memory in children with CIs compared with their NH age mates?
(Lachman et al. 1979). Specifically, the ability to process and
(2) Does the potential for verbal recoding affect performance on measures
of reasoning ability in children with CIs relative to their NH age mates? store information in immediate memory contributes to devel-
and (3) Is performance on verbal and visuospatial working memory tasks opment of both verbal and visuospatial reasoning abilities and
related to spoken receptive language level achieved by children with CIs? ultimately language and academic performance (Alloway et al.
2006). This ability may be impaired in children born with severe
Design: A total of 54 children ranging in age from 5 to 9 years partici- to profound hearing loss who experience auditory deprivation
pated; 25 children with CIs and 29 children with NH. Participants were
during early developmental years critical for development of
tested on both simple and complex measures of verbal and visuospatial
working memory. Vocabulary was assessed with the Peabody Picture skills that are dependent on the processing of verbal information.
Vocabulary Test (PPVT) and reasoning abilities with two subtests of the The sensory deficit imposed by hearing loss in these children
WISC-IV (Wechsler Intelligence Scale for Children, 4th edition): Picture (even when remediated with CIs) typically results in delays in
Concepts (verbally mediated) and Matrix Reasoning (visuospatial task). spoken language (Osberger 1986; Svirsky et al. 2004; Bingham
Groups were compared on all measures using analysis of variance after et al. 2009; Geers et al. 2009). Children who receive CIs in early
controlling for age and maternal education. childhood represent a group of children who gain partial access
Results: Children with CIs scored significantly lower than children with to auditory speech information at some point during this critical
NH on measures of working memory, after accounting for age and mater- developmental period. Whether this altered sensory input affects
nal education. Differences between the groups were more apparent for only verbal processing and language or whether a more general
verbal working memory compared with visuospatial working memory. deficit affects both verbal and visuospatial memory/reasoning
For reasoning and vocabulary, the CI group scored significantly lower has been the subject of some debate in the literature, particularly
than the NH group for PPVT and WISC Picture Concepts but similar to with regard to the process known as working memory.
NH age mates on WISC Matrix Reasoning. Working memory refers to an individual’s capacity to store
Conclusions: Results from this study suggest that children with CIs and manipulate information for short periods of time (Alloway
have deficits in working memory related to storing and processing ver- et al. 2006). A widely accepted model of working memory
bal information in working memory. These deficits extend to receptive developed by Baddeley and Hitch (1974) proposes that work-
vocabulary and verbal reasoning and remain even after controlling for ing memory is under the control of a domain general attention
the higher maternal education level of the NH group. Their ability to store system referred to as the central executive. The central execu-
and process visuospatial information in working memory and complete tive is responsible for coordinating activity of two subsystems
reasoning tasks that minimize verbal labeling of stimuli more closely for short-term storage of verbal and visuospatial information
approaches performance of NH age mates.
(phonological loop and visuospatial sketchpad, respectively).
(Ear & Hearing 2018;XX;00–00) The tasks designed to assess working memory skills may be
classified as simple versus complex; simple tasks primarily require
INTRODUCTION storage (i.e., serial recall of digits or words), while complex tasks
require coordination of both storage and processing (e.g., adding
Pisoni et al. (2016) have long advocated using information- a task that requires the participant to identify and verbally name
processing models developed by cognitive psychologists to colors of digits that are to be serially recalled; Engle et al. 1999;
explain variability in spoken language outcomes in pediatric Hale et al. 2011; Ead et al. 2013). Tasks have been developed to
cochlear implant (CI) recipients. Under these models, human measure both simple and complex memory processes in the verbal
behaviors are assumed to involve a hierarchical sequencing of and visuospatial domains, depending on the nature of the stimuli
(Baddeley & Logie 1999; Cocchini et al. 2002).
1
Department of Otolaryngology, Washington University School of
Medicine, St. Louis, Missouri, USA; 2Department of Behavioral and Brain
Sciences, University of Texas Dallas, Dallas, Texas, USA; 3Department of
Assessment Considerations
Psychology, Washington University St. Louis, Missouri, USA; and 4Moog The verbal working memory system is responsible for stor-
Center for Deaf Education, St. Louis, Missouri, USA. ing information that is expressed in spoken language (e.g.,

0196/0202/2018/XXXX-00/0 • Ear & Hearing • Copyright © 2018 Wolters Kluwer Health, Inc. All rights reserved • Printed in the U.S.A.

1
Copyright © 2018 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.
<zdoi; 10.1097/AUD.0000000000000629>
2 Davidson et al. / EAR & HEARING, VOL. XX, NO. XX, 00–00

numbers, words, and sentences). An important consideration strategies.” They subsequently conclude that deficits in verbal
for assessing verbal working memory is ensuring that the ver- working memory abilities are not due to reduced audibility or
bal items to be remembered are encoded (i.e., perceived) accu- speech production capabilities, rather children with CIs are less
rately. One way to guarantee that a participant has correctly efficient at using phonological and linguistic strategies to main-
encoded each item in a verbal series is to have them repeat each tain and process verbal information.
item out loud. Other studies reporting similar deficits in verbal working
The visuospatial working memory system is responsible for memory for CI recipients have used serial recall of nonwords
storing information related to locations or sequences of objects or nonword word repetition to estimate storage (simple task)
or images. An important consideration for assessing visuospa- and sentence completion and recall to estimate storage and pro-
tial working memory is ensuring the task has eliminated the cessing (complex task; Lyxell et al. 2008; Wass et al. 2008).
possibility of verbal mediation. Thus, it is important that no ver- The majority of these presented the stimuli so that the par-
balization be permitted and that the reporting of the responses is ticipant could both hear the talker and see their face and the
spatial. Tasks that use sequencing of colors or objects may offer participants’ responses were verbal. In a departure from the
opportunities for verbal recoding of stimuli (Archibald & Gath- tasks described previously, Nittrouer et al. (2013, 2017) used
ercole 2006). That is, children may use learning strategies (i.e., a single serial recall task to obtain separate estimates of stor-
verbal rehearsal) to help maintain items in working memory and age and processing (i.e., simple and complex) in verbal work-
aid in their recall. If opportunities for verbal recoding are pres- ing memory. Pediatric CI recipients were required to listen to
ent, assessment of visuospatial working memory as separate closed sets of rhyming and nonrhyming nouns and adjectives
from verbal working memory may be compromised (Poppen and respond by tapping pictures arranged on a computer screen
et al. 1969; Wyke & Asso 1979; Montgomery 1993). in the same order as they were presented. They hypothesized
that nonrhyming words would be recalled with greater accu-
Verbal Working Memory in Children With CIs racy because they are more phonologically distinct and would
Consistent with the hypothesis that an impoverished audi- have more robust representations in storage. Thus, differences
tory sensory input disrupts accurate encoding of verbal infor- in accuracy of recall of rhyming and nonrhyming words would
mation necessary for phonological processing and memory, assess storage capacity. They suggest that nouns require less of
several studies have found that children with CIs exhibit poorer a processing load than adjectives because nouns can be readily
performance than their normal hearing (NH) age mates on tests represented with an actual item or picture, whereas adjectives
of both simple and, in some cases, complex verbal working must be inferred from a picture. They hypothesized that rate of
memory (Pisoni & Geers 2000; Pisoni & Cleary 2003; Watson recall would index processing with the expectation that adjec-
et al. 2007; Kronenberger et al. 2013). For example, this result tives would have longer response rates due to greater process-
is seen with forward and backward digit span tasks, widely ing demands. Using two separate experiments on adults and
used for evaluating short-term (simple forward span task) and children, respectively, they found that accuracy was poorest for
working (complex backward span task) memory in NH chil- the rhyming words and recall was much slower for the adjec-
dren (Pisoni & Geers 2000; Burkholder & Pisoni 2003; Watson tives. They also reported that correlations between accuracy and
et al. 2007; Pisoni et al. 2011; Harris et al. 2013; Kronenberger response time were not significant, confirming that these mea-
et al. 2013). Accurate encoding of verbal stimuli may be an sures represent different abilities. The authors concluded that
issue for children with hearing loss, especially when stimuli are storage and processing (simple and complex working memory)
presented auditorily. Lower performance by children with CIs could be assessed separately using a single task. A group of CI
compared with age mates with NH may be related to dimin- recipients and age mates with NH were tested at second grade
ished audibility and/or poorer frequency resolution. More- (Nittrouer et al. 2013) and again 2 years later at fourth grade
over, speech production difficulties of children with CIs may (Nittrouer et al. 2017). At the second-grade test session, the CI
prohibit clear and accurate verbal responses. To address these recipients performed significantly worse than age mates with
issues, AuBuchon et al. (2015) designed tasks that were likely NH on accuracy but similar on rate of responding (on accurately
to minimize the effects of poor audibility/frequency resolu- recalled items). However, at the fourth-grade test session, the
tion and speech production issues for children with CIs. The CI recipients performed more poorly on accuracy (fewer items
digit span tasks were administered using both visual and audi- recalled correctly) and they exhibited slower reaction times. The
tory presentation of stimuli and both verbal (i.e., spoken recall) authors concluded that children with CIs exhibited verbal work-
and nonverbal (i.e., touch screen) responses. They found that ing memory deficits related to both storage and processing.
the NH group performed better than the CI group on forward Furthermore, at the second test session, they found the major
digit span regardless of presentation mode or response modal- source of variability for verbal working memory abilities dif-
ity. Both children with NH and children with CIs performed fered for the NH and CI groups. The major source of variability
more poorly on backward digit span than forward. However, the for verbal working memory was phonological awareness for the
differences between the groups on backward span were not sta- NH group and vocabulary for the CI group.
tistically different. The authors suggest that the lack of a statis-
tically significant difference between the 2 groups for complex Visuospatial Working Memory in Children With CIs
span may be related to lack of statistical power to detect true Assessment of visuospatial working memory may be con-
differences. They also suggest that reversing the order of dig- founded by verbal demands of the experimental task (Archibald
its makes the task more difficult for both groups; however, this & Gathercole 2006). This was apparent in an early study that
may be “particularly detrimental for the NH controls because found that pediatric CI recipients had shorter spans for loca-
it also interferes with their ability to initiate lexical processing tions of color sequences presented through visual cues alone

Copyright © 2018 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.
Davidson et al. / EAR & HEARING, VOL. XX, NO. XX, 00–00 3

than was observed in age mates with NH sensitivity (Cleary different methodologies (i.e., learning accuracy versus reaction
et al. 2001). Subsequent studies addressing visuospatial work- times) and to the extent to which nonverbal stimuli may be ver-
ing memory in children with CIs have predominantly used tasks bally mediated.
to assess simple working memory that are not subject to verbal
encoding (Lyxell et al. 2008; Wass et al. 2008; Conway et al. Importance of Working Memory for Language
2011). These studies used various versions of matrix pattern Development
or dot location tasks that require the subject to view patterns
Reaching developmental milestones in speech and language
of filled matrices or dot locations on a computer screen for a
at a rate commensurate with typically developing children
short period of time and then replicate the pattern or locations
with NH sensitivity is supported by verbal working memory
on an empty matrix. In some cases, the number of locations
abilities (Gathercole et al. 1997; Adams & Gathercole 2000;
or patterns to be recalled increases until the subject reaches a
Alloway et al. 2009). Moreover, several studies with pediatric
ceiling performance level. The majority of these tasks do not
CI recipients have demonstrated that verbal working memory
require items to be recalled in a specific order (i.e., serial recall).
abilities are correlated with spoken language outcomes (Pisoni
In a departure from typical visuospatial tasks, an earlier study & Geers 2000; Pisoni & Cleary 2003; Ibertsson et al. 2009).
of pediatric CI recipients used a task that required subjects to More recently, Marschark et al. (2015) demonstrated that spatial
replicate alternating hand movements (fist versus palm) in the processing in deaf individuals is more highly associated with
order they were presented (Dawson et al. 2002). In the afore- language ability than in a NH population, and this relation is
mentioned studies, children with CIs performed on par with independent of the child’s preferred mode of communication
their age mates with NH sensitivity. (sign or speech). These findings suggest that strong working
The communication backgrounds of children from these memory skills may serve an important function in language
studies have varied with some reporting exposure to spoken acquisition in children, but visuospatial memory may be more
language exclusively (Dawson et al. 2002) and others reporting critical in the case of children with hearing loss.
some exposure to sign language before receiving a CI (Lyxell
et al. 2008; Wass et al. 2008; Conway et al. 2011). Interestingly,
reliance on sign language has been associated with superior Verbal and Visuospatial Reasoning Abilities in Children
performance, compared with reliance on spoken language, on With CIs
tasks requiring visuospatial memory (Marschark 2006). A sub- The accurate assessment of cognitive abilities in children
sequent study, however, failed to demonstrate a similar advan- with hearing loss is dependent on minimizing the effects of
tage for sign language users (Marschark et al. 2015). auditory and language deficits (Phillips et al. 2014) by using
visual-motor and visuospatial (i.e., nonverbal) tasks. Tasks that
require a child to solve problems by drawing upon visual-motor
Auditory Deprivation and Sequential Processing and visuospatial skills are thought to provide an overall estimate
Some researchers (e.g., Conway et al. 2011) propose that of general cognitive abilities in children with normal hearing
experience with the temporal nature of sound signals affects (Cattell 1987) and children with hearing loss perform similarly
how individuals learn and process serial input. Lack of audi- to age mates with NH on such tasks (Krivitski et al. 2004; Khan
tory experience by children with hearing impairment may et al. 2005; Zekveld et al. 2007). Cognitive assessments that
disrupt temporal processing from both auditory and visual have not controlled for the effects of auditory and verbal skills
modalities (e.g., visual sequence learning) and may result in may underestimate nonverbal cognitive skills of children with
global changes in neurocognitive functions (Pisoni et al. 2016). hearing loss (Braden 1992; van Boxtel et al. 2000; Phillips et al.
These researchers propose a domain-general delay on working 2014). Castellanos et al. (2015) compared visual concept for-
memory tasks that require sequential processing, whether stim- mation skills of a group of 57 long-term CI users to 71 NH
uli are presented in visual or auditory modalities. Khan et al. peers. The CI participants ranged in age from 7 to 27 years, had
(2005) found that children with hearing aids (HAs) exhibited received a CI before age 7, and had used their CI for at least 7
poorer performance than children with NH and children with years. The majority (~63%) of participants used a unilateral CI
CIs on tasks that required sequential ordering of visual stimuli. only (i.e., no device at the nonimplanted ear). The communi-
Another study found that children with CIs performed signif- cation mode for these CI participants varied from mostly sign
icantly below published norms on a task that required visual to auditory verbal only. Concept formation tasks were adminis-
monitoring of sequentially presented visual stimuli (Horn et al. tered to assess the ability to respond to a common set of features
2005). More recent studies of adult and pediatric CI recipi- to classify objects or events. Study participants were asked to
ents report delays in both visual and motor sequence-learning identify and verbalize the underlying rule for grouping objects.
or processing skills (Lévesque et al. 2014; Ulanet et al. 2014; Rules for grouping could be related to size, quantity, shape, or
Bharadwaj & Mehta 2016). Yet in other studies in which stim- color and were distributed across three categories; single com-
uli were carefully designed to preclude the use of overlearned parison and single rule, multiple comparisons and single rule,
labels (e.g., colors) that could be verbally rehearsed, CI recipi- and multiple comparisons and multiple rules. They found that
ents and NH age mates exhibited similar sequential learning CI recipients performed significantly poorer on concept for-
abilities (Torkildsen et al. 2018; Hall et al. 2018). Moreover, mation tasks, especially when multiple comparisons and rules
some studies of children with CIs have found that performance were involved. They also found that concept formation skills
on nonverbal and visual tasks requiring sequential processing of were more strongly related to vocabulary skills for the CI group
stimuli is associated with spoken language skills (Dawson et al. compared with the NH group. The authors concluded that early
2002; Edwards & Anderson 2014; Ulanet et al. 2014). Differ- auditory deprivation combined with an impoverished auditory
ences in general trends across studies may be due, in part, to signal from a CI affect higher order cognitive skills including

Copyright © 2018 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.
4 Davidson et al. / EAR & HEARING, VOL. XX, NO. XX, 00–00

conceptual reasoning. While the stimuli in the aforementioned TABLE 1. Audiological characteristics of participants, listed
study were nonverbal, the participants were required to verbal- first for the full sample, then followed by means for each device
ize their responses. Thus, to the degree that these tasks require group, bilateral and bimodal
some degree of verbal mediation, children with hearing loss Mean SD n
may score lower than age mates with NH.
Age first HA (mo) 16.8 9.4 24
 Bilateral CIs (2 CIs) 16.2 8.2 17
Objectives of the Current Investigation  Bimodal devices (1 HA and 1 CI) 18.1 12.3 7
The principal goal of this study was to compare working Age at first CI (mo) 30.1 15.7 25
memory in children using CIs with their NH age mates, using  Bilateral CIs (2 CIs) 25.2 13.5 18
both simple and complex tasks in both verbal and visuospatial  Bimodal devices (1 HA and 1 CI) 42.7 14.8 7
domains. This study only included subjects who relied on spo- Pre-CI unaided PTA (dB HL) first 107.1 11.1 24
ken communication to control for possible influence of sign CI ear
language proficiency on visuospatial working memory. The  Bilateral CIs (2 CIs) 107.1 11.8 17
 Bimodal devices (1 HA and 1 CI) 107.2 10.2 7
main questions addressed by this study were (1) Does auditory
Pre-CI unaided PTA (dB HL) second 94.5 18.3 24
deprivation result in global or domain-specific deficits in work-
ear
ing memory in children with CIs compared with their NH age  Bilateral CIs (2 CIs) 98.1 18.4 17
mates? (2) Does the potential for verbal recoding affect perfor-  Bimodal devices (1 HA and 1 CI) 85.8 15.8 7
mance on measures of reasoning ability in children with CIs
relative to their NH age mates? and (3) Is performance on ver- CI, cochlear implant; HA, hearing aid.
bal and visuospatial working memory tasks related to spoken
receptive language level achieved by CI children? group had their loss first identified at age 10 months (SD = 10),
To address these questions, children with NH and CIs were although for 5 children the age at identification was unknown.
tested on both simple and complex measures of verbal and visuo- They received their first HAs at an average age of 16.8 months
spatial working memory. A receptive vocabulary test and two (SD = 9.4) and their first CI at 30 months of age (SD = 15.7).
tests of perceptual reasoning abilities were also administered. Approximately half (52%) of the participants reported the eti-
ology of the hearing loss as unknown and the other half was
MATERIALS AND METHODS nearly equally distributed across Connexin, enlarged vestibular
aqueduct, and syndromic.
Fifty-four children ranging in age from 5 to 9 years partici-
All children with CIs had open-set word recognition and
pated: 25 children with CIs and 29 children with NH. There were
aided threshold testing completed as part of their audiology care
10 females in the CI group and 14 females in the NH group.
within 15 months of the test date for the study. Open-set speech
All children were recruited from the local metropolitan area in
perception tests were administered at a conversational level
St. Louis, Missouri (USA). Children with CIs were recruited
of 60 to 65 dB SPL using one of the following word lists: the
through local CI surgical centers and a private oral school for
Lexical Neighborhood Test (LNT; Kirk et al. 1995), the Conso-
the deaf. Children with NH were recruited from local grade
nant Nucleus Consonant (CNC) word lists (Peterson & Lehiste
schools. All 25 children with CIs had parents with NH sensi-
1962), or the Phonetically Balanced Kindergarten Wordlist
tivity and received educational services via spoken language
(PBK; Haskins, Reference Note 1). The majority of the children
(English) in either a general public education setting or an audi-
had received the LNT (n = 19), followed by the CNC (n = 5) and
tory-oral private school for the deaf. None of the children were
the PBK (n = 1). The average speech perception score across
reported to have any delays in cognitive development. Maternal
all tests was 77% (SD = 16) correct. The average LNT score
education level was used as a sociodemographic variable and
was 75% (SD = 12), the CNC score was 81% (SD = 12), and
calculated in total years of education through college or beyond.
the PBK score was 96%. All children had aided threshold PTAs
The average educational level was 16.8 years (SD = 1.9) for the
(at 0.5, 1, and 2 kHz) ≤30 dB HL. Before testing in the cur-
NH group and 15 years (SD = 2.6) for the CI group. The aver-
rent study, all devices were checked for proper functioning by a
age age at test was 7.9 years (SD = 1.6) for the CI group and
certified pediatric audiologist. Testing was conducted in a quiet
7.4 years (SD = 1.7) for the NH group. Over 80% of both the CI
testing suite in the research lab, and all testing was conducted
and NH groups were Caucasian. The only significant difference
by a single examiner under the supervision of a certified cogni-
in demographic variables between the CI and NH groups was
tive psychologist.
mother’s education level, F(1,52) = 8.21; p < 0.01.
A total of 18 children used bilateral CIs (CI at each ear),
and 7 used bimodal devices (CI with a HA at the nonimplanted Test Measures
ear). The audiologic data for the total group and for the bilateral Verbal working memory and visuospatial working memory
and bimodal groups separately are shown in Table 1. Note on were assessed using both simple and complex versions of the
Table 1 that data for age at HA was unavailable for one partici- tasks. Simple tasks required serial recall of visually presented
pant and unaided pre-CI pure-tone average (PTA) for another items, while complex tasks required serial recall of items while
participant. The only significant difference between the bilat- performing a secondary task (i.e., counting geometric shapes or
eral and bimodal CI groups was age at first CI, F(1,23) = 8.06; recalling location of different shape on grid). A pictorial repre-
p < 0.01. The bilateral group received their first CI at an ear- sentation of each task is shown in Figure 1.
lier age than the bimodal group. There were no significant dif- Simple Verbal Working Memory—(Digit Span) • For this
ferences between the 2 CI groups for age at test, age at first task, participants watched a series of two to seven digits presented
HA, or any of the calculated unaided PTAs. The combined CI on a computer screen. Each digit of a given series was presented

Copyright © 2018 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.
Davidson et al. / EAR & HEARING, VOL. XX, NO. XX, 00–00 5

Fig. 1. Pictorial representations of the tasks for (A) simple verbal working memory, (B) complex verbal working memory, (C) simple visuospatial working
memory, and (D) complex visuospatial working memory.

individually, and participants were instructed to repeat each digit four trials was required to proceed to the next higher counting
out loud when it appeared on the screen. Digits were on the screen series. A practice trial of three counting series was given before
for 2000 msec with an interstimulus interval of 500 msec. A green the test was initiated. Memory span was calculated by taking the
box was illuminated at the completion of each digit series to sig- longest counting span at which the participant correctly recalled
nal the participant to repeat the digits out loud in the order they three out of four trials.
appeared. Four trials were presented for each digit series; correct Simple Visuospatial Working Memory—(Location
serial recall of three out of the four trials was required to proceed Span)  •  For this task, participants watched a computer screen
to the next series length (e.g., from two to three digits). A practice with a 4 × 4 grid and touched the location on the grid with a red
trial of a three-digit series was given before the test was initiated. circle. Upon touching the location, the circle disappeared, and
Memory span was calculated by taking the longest digit span at another screen with a circle in a different grid location was pre-
which the participant correctly recalled three out of four trials. sented. Participants were told to remember the location of the
Complex Verbal Working Memory—(Counting Span)  • For circle for each screen and when the green go box was illuminated
this task, participants watched a computer screen with an array to touch the locations of the circles on the grid in the order that
of geometric shapes that consisted of triangles and circles. The they appeared. The number of locations to be remembered ranged
primary task was to remember the total counts associated with from two to seven. Four trials were presented for each location
each screen, and the secondary task was to count the triangles series length; correct serial recall of three out of the four trials
out loud. Participants watched individual screens with numbers was required to proceed to the next series length. A practice trial
of circles ranging from two to seven and were told to count the of three location series was given before the test was initiated.
shapes out loud and repeat (out loud) the total number counted Memory span was calculated by taking the longest location span
for each screen. When signaled by the green go box, they were at which the participant correctly recalled three out of four trials.
told to repeat the numbers counted per screen out loud, in the Complex Visuospatial Working Memory—(Odd-One-Out
order they appeared. Four trials were presented for each count- Location Span)  •  For this task, participants watched a com-
ing series (two to seven); correct serial recall of three out of the puter screen with various geometric shapes placed in a 4 × 4

Copyright © 2018 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.
6 Davidson et al. / EAR & HEARING, VOL. XX, NO. XX, 00–00

grid. Each to be remembered location appeared on the screen as RESULTS


a unique shape accompanied by two irrelevant locations filled
Statistical Analyses
with two identical shapes (different from the target). The partici-
Analysis of variance was used to compare group differences
pant was instructed to identify (and touch) the unique shape and
on all outcome measures (working memory, PPVT, WISC Pic-
then recall, in serial order, the touched locations only when the
ture Concepts, and WISC Matrix Reasoning). Correlational
green go box was illuminated. The primary task is to remember
analyses were used to examine associations between possible
the location of the “touched items,” and the secondary task is
device and demographic variables and all outcome variables, as
to “find and touch” the odd-one-out. The number of locations
well as working memory variables and vocabulary and verbal
to be remembered ranged from two to seven. Four trials were
reasoning outcomes.
presented for each location series; correct serial recall of three
out of the four trials was required to proceed to the next higher
level. A practice trial of three location series was given before Selection of Predictor Variables
the test was initiated. Memory span was calculated by taking the Within the CI group, correlations between audiological vari-
longest location span at which the participant correctly recalled ables (unaided PTAs, age at first HA, and age at CI) and all
three out of four trials. outcome measures (verbal working memory, visuospatial work-
The Picture Concepts and Matrix Reasoning subtests ing memory, PPVT, WISC Picture Concepts, and WISC Matrix
from the Wechsler Intelligence Scale for Children, 4th edi- Reasoning) were not significant (r-value range,−0.33 to 0.17; p
tion (WISC-IV; Wechsler 2003), were used to assess over- > 0.05), so these variables were not included in further analy-
all perceptual (fluid) reasoning abilities. The WISC Picture ses. There were no significant differences between data for the
Concepts and Matrix Reasoning tasks were chosen to rep- bimodal and bilateral CI users on any outcome measure (verbal
resent tasks that differ in the extent to which verbal skills working memory, visuospatial working memory, PPVT, WISC
may be required to solve visual and visuospatial problems. Picture Concepts, and WISC Matrix Reasoning). On the basis
WISC Picture Concepts measures perceptual organization of of these results, further analyses comparing outcome measures
nonverbal concepts (i.e., organize and categorize common in the NH and CI groups were conducted with the 2 CI groups
features of nonverbal concepts). For this subtest, the par- combined.
ticipants were presented with two to three rows of pictures Age at test was significantly correlated with all outcome
and asked to select one picture from each row that related measures (r-value range, 0.43 to 0.71; p < 0.01) and was used
conceptually to one another. For example, the child sees one as a covariate for all group comparisons. Correlations between
row with a picture of a car and a picture of a book, and the mother’s education and all outcome measures were not signifi-
second row shows a picture of the sun and a picture of a bus. cant except for PPVT (r = 0.47; p < 0.01). However, due to the
The child should point to the car and the bus because they are significant difference between CI and NH groups in this vari-
both modes of transportation. The number of items in each able, group comparisons were conducted with maternal educa-
row and the numbers of rows increase as the test progresses. tion controlled.
For example, the child is presented with three rows with Conversion to Standardized Scores • To compare across
three pictures in each row. The child should choose (point WM measures with different distributions, raw scores were
to) the bathtub, fire-hydrant and water hose, because all use converted to z scores based on the distribution of scores in the
water. Although stimulus presentation and response demands CI and NH groups combined. Age norms were not available
are nonverbal, accurate responses require verbal reasoning. on the WISC (Picture Concepts and Matrix Reasoning) for the
The child receives 1 point for each correct answer. Testing youngest children in this study so for comparable age correc-
stops after five consecutive incorrect answers. The WISC tion, raw scores were converted to z scores for these subtests as
Matrix Reasoning subtest measures a child’s skill at grasp- well. Table 2 includes the mean and SDs for the raw scores and
ing shapes, designs, and visuospatial patterns to identify or z scores for all tasks; verbal and visuospatial working memory
correct missing aspects of these concepts and complete or (simple and complex), PPVT, and Picture Concepts and Matrix
correct them. For this subtest, the child is presented with a Reasoning from the WISC.
series of incomplete matrices, each of which is a series of Analysis of Covariance  • The z scores for the working memory
abstract patterns and designs. The child is directed to select tasks were analyzed using a mixed model analysis of variance
the best from five item choices to complete the matrix. For with age at test and maternal education entered as a covariates
example, the child is shown colored matrices or visual pat- (ANCOVA) to adjust for the difference in maternal education
terns with something missing and asked to select the missing between the CI and NH groups and age-related differences
piece from a range of options. The child receives 1 point for across the participants. A significant effect for age was found
each correct answer. Testing stops after 4 consecutive incor- [F (1,50) = 50.74; p < 0.001]; however, there was no significant
rect answers. effect for maternal education [F (1,50) = 1.06; p > 0.05]. Group
The Peabody Picture Vocabulary Test-III • The Peabody (NH versus CI) was entered as a between-subjects’ variable, and
Picture Vocabulary Test (PPVT; Dunn & Dunn 1997) was used domain (verbal versus visuospatial) and task difficulty (simple
as a measure of receptive vocabulary for children in both the versus complex) were entered as within-subject variables.
CI and NH groups. The test was administered face to face. The Results revealed a main effect for group [F(1,50) = 10.03; p <
child was instructed to select the picture that best represented 0.01]. Cohen d effect size was 0.90. There were no significant
the spoken target word from four alternatives. The raw score interactions. To test the validity of the normality assumption
corresponds to the number of items below a basal level (7 con- for data, the residuals from the ANCOVA model were exam-
secutive correct responses) plus the number of items correctly ined to control for systematic between-groups variability. Due
selected. to multiple error terms (i.e., multiple within-subjects linear

Copyright © 2018 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.
Davidson et al. / EAR & HEARING, VOL. XX, NO. XX, 00–00 7

TABLE 2.  Group mean and SD values for all measures

Simple Verbal Simple Visuospatial Complex Verbal Complex


Span Span Span Visuospatial Span
Raw scores n Mean SD Mean SD Mean SD Mean SD
 CI 25 3.0 0.8 2.8 1.1 2.2 0.9 1.9 1.1
 NH 29 3.9 1.5 3.1 1.3 2.8 1.1 2.2 1.0
z scores Mean SD Mean SD Mean SD Mean SD
 CI 25 −0.39 0.64 −0.12 0.89 −0.32 0.85 −0.15 1.07
 NH 29 0.34 1.14 0.10 1.09 0.28 1.05 0.13 0.94
WISC-PC WISC-MR PPVT
Raw scores Mean SD Mean SD Mean SD
 CI 25 13.4 3.3 16.6 5.9 104.1 24.8
 NH 29 15.1 4.4 17.3 5.9 140.1 20.2
z scores Mean SD Mean SD Mean SD
 CI 25 −0.23 0.8 −0.06 1.0 −0.67 0.9
 NH 29 0.19 1.1 0.05 1.0 0.58 0.7

CI, cochlear implant; NH, normal hearing; PPVT, Peabody Picture Vocabulary Test; WISC-MR, Wechsler Intelligence Scale for Children Matrix Reasoning test; WISC-PC, Wechsler Intelligence
Scale for Children Picture Concepts test.

combinations), several residual terms were checked for normal- (PPVT, WISC Picture Concepts, and WISC Matrix Reason-
ity. Results from the Shapiro–Wilk test (p > 0.05) revealed that ing) to examine whether the contribution of memory span (ver-
all residuals (domain, difficulty, and Difficulty × Domain) were bal and visuospatial) varied based on the extent of verbal task
normally distributed. demands. Simple verbal working memory scores showed posi-
The z scores for the PPVT, WISC Matrix Reasoning, and tive significant correlations with the PPVT (partial correlation r
WISC Picture Concepts were each compared between the 2 = 0.39; p < 0.004); however, the correlations for WISC Picture
groups (CI and NH) using an ANCOVA with age at test and Concepts were not statistically significant. Simple visuospatial
maternal education entered as a covariates. Results from the working memory scores were positively correlated with WISC
Shapiro–Wilk test (p > 0.05) revealed that the PPVT and WISC Matrix Reasoning (partial correlation 0.48; p < 0.004) but not
Picture Concept, and WISC Matrix Reasoning data were nor- with PPVT scores nor WISC Picture Concepts scores. None
mally distributed. of the correlations between the complex measures of working
Older children outperformed younger children on all three memory (visuospatial and verbal) and vocabulary or reasoning
outcomes: [PPVT, F(1,50) = 33.9, p < 0.001; WISC Picture outcomes (PPVT, WISC Picture Concepts, and WISC Matrix
Concepts, F(1,50) = 41.1, p < 0.001; WISC Matrix Reasoning, Reasoning) were statistically significant.
F(1,50) = 62.8, p < 0.001]. Maternal education was only signifi-
cant for the PPVT outcome [F(1,50) = 9.99; p < 0.01). The NH
group outperformed the CI group for PPVT [F(1,50) = 44.61; DISCUSSION
p < 0.001] and for WISC Picture Concepts [F(1,50) = 4.53; p < The principal goal of this study was to examine the effects
0.05]; however, there were no significant differences for WISC of early auditory deprivation on cognitive function in the verbal
Matrix Reasoning [F(1,50) = 0.078; p > 0.05]. Cohen d effects and visuospatial domains by addressing three questions.
sizes were 1.58 and 0.43 for the PPVT and WISC Picture Con-
cepts, respectively.
Comparing Verbal and Visuospatial Domains • Results Does Early Auditory Deprivation Result in Global
of z score comparisons indicated that CI users exhibited sig- or Domain-Specific Deficits in Working Memory in
nificantly lower performance relative to NH peers on tasks that Children With CIs Compared With Age Mates Who
required some degree of verbal processing (verbal working Have NH?
memory, WISC Picture Concepts, and PPVT) and exhibited The results from this study suggest that working memory
similar performance on visuospatial processing tasks (visuospa- deficits in children with CIs are domain specific. That is, they
tial working memory and WISC Matrix Reasoning). Figure 2A are related to deficits in encoding, storing, and manipulating
summarizes the mean z scores and 95% confidence intervals for spoken verbal information. These deficits are at least partially
the CI and NH groups for verbal processing tasks and Figure 2B due to the spectrally degraded auditory signal provided by the
for visuospatial tasks. These scores have been adjusted for age cochlear implant. Overall, the children with CIs scored sig-
and maternal education. Overlapping distributions for CI and nificantly lower on both simple and complex verbal working
NH children are apparent for visuospatial tasks compared with memory tasks compared with their age mates with NH; how-
the relative separation of distributions for the verbal tasks. ever, their performance on measures of visuospatial working
Correlations  •  Table 3 shows partial correlations between memory tasks was similar to NH peers.
working memory spans and outcome measures controlling for Verbal working memory deficits for this CI group persist even
age at test and maternal education. Bonferroni corrections for with good audibility (aided thresholds ≤ 30 dB HL). Aided detec-
12 comparisons required a p value of < 0.004 for significance. tion thresholds for CI users that are ≤ 30 dB HL or better from 250
Correlations were calculated between measures of working to 4000 Hz have been shown to be associated with better speech
memory and measures of vocabulary and perceptual reasoning perception scores and spoken language outcomes for both adult and

Copyright © 2018 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.
8 Davidson et al. / EAR & HEARING, VOL. XX, NO. XX, 00–00

Fig. 2. Means and 95% confidence intervals for z scores for normal-hearing (NH) and cochlear implant (CI) groups for simple verbal working memory longest
span, complex verbal working memory longest span, Wechsler Intelligence Scale for Children (WISC) Picture Concepts and Peabody Picture Vocabulary Test
(PPVT;A) and simple visuospatial working memory longest span, complex visuospatial working memory longest span, WISC Matrix Reasoning (B).

pediatric CI recipients (Donaldson & Allen 2003; Davidson et al. both audibility and speech production on forward digit span, they
2010, 2014; Holden et al. 2013). Additionally, good open-set speech reported that the NH group performed better than the CI group
recognition had been documented for this group (mean score of regardless of presentation mode or response modality. Alterna-
77% correct). Children in the current study repeated the numbers tively, having the children repeat digits out loud may have allowed
out loud after the presentation of each individual digit (simple task), all children an added opportunity for articulatory rehearsal of digits
and they counted the number of shapes out loud (from each series) for more efficient storage and retrieval from short-term memory.
and repeated the total number counted before being prompted to Despite this opportunity for the CI group to overtly rehearse the dig-
repeat the entire series. This was done to ensure that the younger its, their performance still remained poorer than their NH age mates.
children, especially those with CIs, had identified the digits cor- The NH group outperformed the CI group on both simple and
rectly and counted the shapes accurately. Thus, the CI participants’ complex tasks of verbal working memory, supporting deficits in
performance may have been affected by less efficient production both storage and processing of stimuli in the verbal domain.
skills compared with the NH children. Although recall that when This finding is consistent with other studies reporting similar
AuBuchon et al. (2015) used tasks that minimized the effects of deficits in both storage and processing in the verbal domain

Copyright © 2018 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.
Davidson et al. / EAR & HEARING, VOL. XX, NO. XX, 00–00 9

TABLE 3.  Partial correlations (controlling for age and maternal education) between working memory spans and outcome measures

Partial Correlations

Control Variables SV Span z Score SVS Span z Score CV Span z Score CVS Span z Score
Age and maternal
education PPVT z score Correlation 0.39 0.37 0.37 0.22
Sig (2-tailed) 0.004 0.007 0.007 0.120
df 50 50 50 50
WISC-MR z score Correlation 0.27 0.48 0.30 0.33
Sig (2-tailed) 0.056 0.000 0.028 0.015
df 50 50 50 50
WISC-PC z score Correlation 0.37 0.26 0.35 0.30
Sig (2-tailed) 0.007 0.063 0.011 0.030
df 50 50 50 50

Bonferroni corrections for 12 comparisons require a P value of < 0.0042 for significance. All scores have been converted to z scores to allow for direct comparison in the same units.
Bold font indicates correlations that reach statistical significance.
CV, complex verbal longest span; CVS, complex visuospatial longest span; df, degrees of freedom; PPVT, Peabody Picture Vocabulary Test; SV, simple verbal longest span, SVS, simple visuo-
spatial longest span; WISC-MR, Wechsler Intelligence Scale for Children Matrix Reasoning test; WISC-PC, Wechsler Intelligence Scale for Children Picture Concepts test.

(Pisoni & Geers 2000; Burkholder & Pisoni 2003; Watson et al. verbal deficits were apparent even after controlling for the higher
2007; Pisoni et al. 2011; Harris et al. 2013; Kronenberger et al. level of maternal education of the NH group. Higher levels of
2013) and more recent results from Nittrouer et al. (2017). maternal education have been positively associated with language
In contrast to verbal working memory, the children with CIs in development in typically developing children and children with
the present study were similar to their NH age mates on visuospa- CIs and HAs (Dollaghan et al. 1999; Geers et al. 2009; Niparko
tial working memory tasks, both simple and complex. The results et al. 2010; Ching et al. 2017). Both the quantity and quality of
of the current study are similar to other studies that have shown early linguistic and communicative input provided to the child are
CI recipients perform similarly to NH age mates on tasks that thought to be at least partly responsible for the positive influence
primarily assess storage for visuospatial working memory (Lyxell on spoken language and academic outcomes (Carney & Moeller
et al. 2008; Wass et al. 2008; Conway et al. 2011). Furthermore, 1998; DesJardin & Eisenberg 2007). The group effect remained
even though the visuospatial memory tasks required serial recall significant in the working memory analysis showing that overall
of locations, the performance for the CI group was on par with the group with NH outperformed the group with CIs.
NH age mates. Recall that some propose that lack of early audi- As expected and consistent with other studies in the litera-
tory experience may affect how individuals learn and process ture, the CI group had significantly lower scores on receptive
serial input, in both the auditory and visual domains (Conway vocabulary compared with NH age mates, even after control-
et al. 2011). Thus, children diagnosed with early hearing loss may ling for group differences in maternal education (Blamey et al.
show deficits on tasks that require sequential processing, whether 2001; Fagan et al. 2007; Geers et al. 2016).
stimuli are presented in visual or auditory modalities (Cleary While tests of receptive vocabulary are clearly verbal in
et al. 2001; Horn et al. 2005; Ulanet et al. 2014). This finding may nature, the WISC Picture Concepts and Matrix Reasoning
have resulted from using tasks that allowed for verbal mediation tasks differ in their reliance on verbal encoding. Both are
even though the presentation was visual and the response was designed to assess overall perceptual reasoning abilities by
nonverbal (e.g., presenting sequences of colored lights for recall drawing primarily upon visual and visuospatial skills; how-
when colors are subject to verbal encoding and may advantage ever, WISC Picture Concepts is more likely to draw upon
NH participants). In contrast, the stimuli and response require- verbal mediation skills than WISC Matrix Reasoning. Com-
ments for the visuospatial tasks used in the current study were parison of CI and NH scores for the WISC Matrix Reasoning
carefully constructed to minimize the likelihood of verbal encod- subtest reveals if the opportunity to verbally recode stimuli is
ing of the visual stimuli. For example, the tasks required that the minimized, children with CIs perform similarly to their NH
children point to the location on a 4 × 4 grid with 16 cells; there- age mates. However, on the WISC Picture Concepts subtest,
fore, the ability to verbally label the locations was minimized. the children with CIs scored significantly lower than their age
This is an important issue to address as the type of task and the mates with NH, even though their responses were nonver-
stimuli may influence the strategies participants use to encode, bal (i.e., they pointed to objects from each row that shared
store, and retrieve items in working memory. Thus, the children similar attributes). These results align with those obtained by
with CIs in this study were able to perform on par with their age Castellanos et al. (2015) who found that long-term pediatric
mates when the visuospatial task was designed in such a way that CI recipients performed more poorly than NH age mates on a
minimized any opportunity to verbally encode or label stimuli. visual concept task that required participants to verbalize the
underlying rule for grouping objects. Thus, even though the
children in this study were not required to verbalize results,
Does the Potential for Verbal Recoding Affect they still exhibited deficits in visual reasoning abilities. There-
Performance on Measures of Reasoning Ability in fore, results for reasoning measures were consistent with those
Children With CIs Relative to Their NH Age Mates? obtained with working memory tasks, indicating domain-spe-
Comparisons of group scores on the PPVT support that chil- cific deficits in verbal processing associated with early audi-
dren with CIs have deficits related to the verbal domain. These tory deprivation.

Copyright © 2018 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.
10 Davidson et al. / EAR & HEARING, VOL. XX, NO. XX, 00–00

Is Performance on Verbal and Visuospatial Working improving the quantity and quality of early linguistic input in
Memory Tasks Related to Spoken Receptive Language the home environments may be valuable. Some children may
Level Achieved by CI Children? also benefit from habilitation efforts focused on the use of top-
After controlling for age and maternal education, only sim- down processing (Nittrouer et al. 2013) and effective commu-
ple verbal span was significantly correlated with vocabulary nication strategies (Lyxell et al. 2008). Identifying the unique
scores. Complex verbal span was not significantly correlated effects of both sensory and cognitive abilities on spoken lan-
with vocabulary; however, many of the youngest participants guage function in children with hearing loss will make it pos-
performed poorly on this task; therefore, floor effects may be sible to identify future directions for habilitation and education.
partially responsible for these results. Furthermore, simple and
complex visuospatial working memory spans failed to corre- ACKNOWLEDGMENTS
late significantly with verbally mediated outcomes (i.e., PPVT
and WISC Picture Concepts), although simple visuospatial span This research was supported by the McDonnell Neuroscience Foundation
at Washington University School of Medicine in St. Louis, MO, and
scores were significantly correlated with a reasoning task that National Institute of Deafness and Communication Disorders grant RO1
is considered nonverbal (i.e., WISC Matrix Reasoning). Thus, DC012778. Appreciation is expressed to the 54 students and their parents
visuospatial working memory is not as closely tied to language who graciously gave their time and effort to participate in this study and to
outcomes as verbal working memory. Sarah Fessenden for conducting testing. This research was approved by the
One major limitation to the current study was that the small Human Studies Committee at Washington University School of Medicine
(#201107375).
sample size prohibited a comprehensive analysis of the unique
contributions of verbal and visuospatial working memory to The authors have no conflicts of interest to disclose.
both verbal and nonverbal skills for children with CIs. Several Address for correspondence: Lisa S. Davidson, Washington University
studies have examined how various working memory tasks (ver- School of Medicine, 4560 Clayton Ave, St. Louis, MO 63110, USA. E-mail:
bal and visuospatial) and cognitive measures relate to spoken davidsonls@wustl.edu
language skills, communication skills, and reading for children Received March 22, 2017; accepted April 22, 2018.
with CIs (Lyxell et al. 2008; Ibertsson et al. 2009; Lyxell et al.
2011; Pisoni et al. 2011; Edwards & Anderson 2014). One focus
of future research may be to determine the unique contribution REFERENCES
of verbal and visuospatial working memory/cognitive skills to Adams, A. M., & Gathercole, S. E. (2000). Limitations in working memory:
spoken language outcomes in children with CIs. This may pro- Implications for language development. Int J Lang Commun Disord, 35,
vide insight for targeting children with CIs who are at risk for 95–116.
deficits that extend beyond processing verbal information. Thus, Alloway, T. P., Gathercole, S. E., Kirkwood, H., et al. (2009). The cogni-
tive and behavioral characteristics of children with low working memory.
children with CIs who fail to make significant progress in spo- Child Dev, 80, 606–621.
ken language despite early intervention services and devices may Alloway, T. P., Gathercole, S. E., Pickering, S. J. (2006). Verbal and visuo-
have processing deficits that extend to the visuospatial domain. spatial short-term and working memory in children: Are they separable?
In summary, the results from this study support that chil- Child Dev, 77, 1698–1716.
dren with CIs have domain-specific deficits related to storing Archibald, L. M., & Gathercole, S. E. (2006). Visuospatial immediate
memory in specific language impairment. J Speech Lang Hear Res, 49,
and processing verbal information in working memory. These 265–277.
deficits extend to receptive vocabulary and perceptual reason- AuBuchon, A. M., Pisoni, D. B., Kronenberger, W. G. (2015). Short-
ing. That is, children with CIs exhibited vocabulary and ver- term and working memory impairments in early-implanted, long-term
bal working memory deficits compared with NH age mates cochlear implant users are independent of audibility and speech produc-
and lower scores on a visual perceptual reasoning task when tion. Ear Hear, 36, 733–737.
Baddeley, A., & Logie, L. H. (1999). Working memory: The multiple com-
verbal encoding was required for optimal performance. In con- ponent model. In A. M. P. Shah (Ed.), Models of Working Memory (pp.
trast, their ability to store and process visuospatial information 28–61). New York: Cambridge University Press.
in working memory seems to be intact and on par with their Baddeley, A. D., & Hitch, G. (1974). Working memory. In H. B. Gordon
NH age mates. Additionally, no difference between CI and NH (Ed.), Psychology of Learning and Motivation (Vol. 8; pp. 47–89). New
York, NY: Academic Press.
groups was observed on a reasoning task that required purely Bharadwaj, S. V., & Mehta, J. A. (2016). An exploratory study of visual
visuospatial skills. sequential processing in children with cochlear implants. Int J Pediatr
The extent that memory delays in CI users are specific to Otorhinolaryngol, 85, 158–165.
the verbal domain or generalized to both verbal and visuospa- Bingham, K., Jenstad, L. M., Shahnaz, N. (2009). Longitudinal changes
tial domains may have importance for determining appropriate in real-ear to coupler difference measurements in infants. J Am Acad
Audiol, 20, 558–568.
habilitation strategies. To the degree that diminished sensory Blamey, P. J., Sarant, J. Z., Paatsch, L. E., et al. (2001). Relationships among
input results in a domain-specific verbal deficit, it may be habil- speech perception, production, language, hearing loss, and age in chil-
itated with improved and earlier sensory (i.e., auditory) input dren with impaired hearing. J Speech Lang Hear Res, 44, 264–285.
provided by improved CI-processing strategies that offer greater Braden, J. P. (1992). Intellectual assessment of deaf and hard-of-hearing
people: A quantitative and qualitative research synthesis. School Psy-
fidelity of the speech signal. Language intervention strategies
chology Review, 21, 82–94.
that are designed to expand memory for auditory-verbal infor- Burkholder, R. A., & Pisoni, D. B. (2003). Speech timing and working
mation may also be considered. Moreover, the contribution memory in profoundly deaf children after cochlear implantation. J Exp
of maternal education to vocabulary outcomes highlights the Child Psychol, 85, 63–88.
importance of early linguistic input for language skills. This is Carney, A. E., & Moeller, M. P. (1998). Treatment efficacy: Hearing loss in
children. J Speech Lang Hear Res, 41, S61–S84.
particularly relevant for children with CIs who must also con- Castellanos, I., Kronenberger, W. G., Beer, J., et al. (2015). Concept forma-
tend with early auditory deprivation and a spectrally impover- tion skills in long-term cochlear implant users. J Deaf Stud Deaf Educ,
ished signal from the CI. Early intervention strategies that target 20, 27–40.

Copyright © 2018 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.
Davidson et al. / EAR & HEARING, VOL. XX, NO. XX, 00–00 11

Cattell, R. B. (1987). Intelligence: Its structure, Growth and Action (Vol. Kirk, K. I., Pisoni, D. B., Osberger, M. J. (1995). Lexical effects on spo-
35). New York, NY: Elsevier. ken word recognition by pediatric cochlear implant users. Ear Hear, 16,
Ching, T. Y. C., Dillon, H., Leigh, G., et al. (2017). Learning from the Longi- 470–481.
tudinal Outcomes of Children with Hearing Impairment (LOCHI) study: Krivitski, E. C., McIntosh, D. E., Rothlisberg, B., et al. (2004). Profile anal-
Summary of 5-year findings and implications. Int J Audiol, 57, 1–7. ysis of deaf children using the universal nonverbal intelligence test. J
Cleary, M., Pisoni, D. B., Geers, A. E. (2001). Some measures of verbal and Psychoeduc Assess, 22, 338–350.
spatial working memory in eight- and nine-year-old hearing-impaired Kronenberger, W. G., Pisoni, D. B., Harris, M. S., et al. (2013). Profiles of
children with cochlear implants. Ear Hear, 22, 395–411. verbal working memory growth predict speech and language develop-
Cocchini, G., Logie, R. H., Della Sala, S., et al. (2002). Concurrent per- ment in children with cochlear implants. J Speech Lang Hear Res, 56,
formance of two memory tasks: Evidence for domain-specific working 805–825.
memory systems. Mem Cognit, 30, 1086–1095. Lachman, R., Lachman, J. L., Butterfield, E. (1979). Cognitive Psychology
Conway, C. M., Karpicke, J., Anaya, E. M., et al. (2011). Nonverbal cogni- and Information Processing: An Introduction. Hillsdale, NJ: Lawrence
tion in deaf children following cochlear implantation: Motor sequencing Erlbaum Associates.
disturbances mediate language delays. Dev Neuropsychol, 36, 237–254. Lévesque, J., Théoret, H., Champoux, F. (2014). Reduced procedural motor
Davidson, L. S., Geers, A. E., Brenner, C. (2010). Cochlear implant char- learning in deaf individuals. Front Hum Neurosci, 8, 343.
acteristics and speech perception skills of adolescents with long-term Lyxell, B., Sahlen, B., Wass, M., et al. (2008). Cognitive development in
device use. Otol Neurotol, 31, 1310–1314. children with cochlear implants: Relations to reading and communica-
Davidson, L. S., Geers, A. E., Nicholas, J. G. (2014). The effects of audibil- tion. Int J Audiol, 47(Suppl 2), S47–S52.
ity and novel word learning ability on vocabulary level in children with Lyxell, B., Wass, M., Sahlén, B., et al. (2011). Development of cognitive and
cochlear implants. Cochlear Implants Int, 15, 211–221. reading skills in deaf children with CIs. Cochlear Implants Int, 12(Suppl
Dawson, P. W., Busby, P. A., McKay, C. M., et al. (2002). Short-term audi- 1), S100–S198.
tory memory in children using cochlear implants and its relevance to Marschark, M. (2006). Intellectual functioning of deaf adults and children:
receptive language. J Speech Lang Hear Res, 45, 789–801. Answers and questions. Eur J Cogn Psychol, 18, 70–89.
DesJardin, J. L., & Eisenberg, L. S. (2007). Maternal contributions: Sup- Marschark, M., Spencer, L. J., Durkin, A., et al. (2015). Understanding lan-
porting language development in young children with cochlear implants. guage, hearing status, and visual-spatial skills. J Deaf Stud Deaf Educ,
Ear Hear, 28, 456–469. 20, 310–330.
Dollaghan, C. A., Campbell, T. F., Paradise, J. L., et al. (1999). Maternal Montgomery, J. W. (1993). Haptic recognition of children with specific lan-
education and measures of early speech and language. J Speech Lang guage impairment: Effects of response modality. J Speech Hear Res, 36,
Hear Res, 42, 1432–1443. 98–104.
Donaldson, G. S., & Allen, S. L. (2003). Effects of presentation level on Niparko, J. K., Tobey, E. A., Thal, D. J., et al; CDaCI Investigative Team.
phoneme and sentence recognition in quiet by cochlear implant listeners. (2010). Spoken language development in children following cochlear
Ear Hear, 24, 392–405. implantation. JAMA, 303, 1498–1506.
Dunn, L. M., & Dunn, L. M. (1997). PPVT-III: Peabody Picture Vocabulary Nittrouer, S., Caldwell-Tarr, A., Low, K. E., et al. (2017). Verbal working
Test. Minneapolis, MN: American Guidance Service. memory in children with cochlear implants. J Speech Lang Hear Res,
Ead, B., Hale, S., DeAlwis, D., et al. (2013). Pilot study of cognition in 60, 3342–3364.
children with unilateral hearing loss. Int J Pediatr Otorhinolaryngol, 77, Nittrouer, S., Caldwell-Tarr, A., Lowenstein, J. H. (2013). Working memory
1856–1860. in children with cochlear implants: Problems are in storage, not process-
Edwards, L., & Anderson, S. (2014). The association between visual, non- ing. Int J Pediatr Otorhinolaryngol, 77, 1886–1898.
verbal cognitive abilities and speech, phonological processing, vocabu- Osberger, M. J., Moeller, M. P., Eccarius, M., et al. (1986). Language
lary and reading outcomes in children with cochlear implants. Ear Hear, and learning skills of hearing-impaired students. Introduction. ASHA
35, 366–374. Monogr, 23, 3–5.
Engle, R. W., Tuholski, S. W., Laughlin, J. E., et al. (1999). Working mem- Peterson, G. E., & Lehiste, I. (1962). Revised CNC lists for auditory tests. J
ory, short-term memory, and general fluid intelligence: A latent-variable Speech Hear Disord, 27, 62–70.
approach. J Exp Psychol Gen, 128, 309–331. Phillips, J., Wiley, S., Barnard, H., et al. (2014). Comparison of two nonver-
Fagan, M. K., Pisoni, D. B., Horn, D. L., et al. (2007). Neuropsychological bal intelligence tests among children who are deaf or hard-of-hearing.
correlates of vocabulary, reading, and working memory in deaf children Res Dev Disabil, 35, 463–471.
with cochlear implants. J Deaf Stud Deaf Educ, 12, 461–471. Pisoni, D. B., & Cleary, M. (2003). Measures of working memory span and
Gathercole, S. E., Hitch, G. J., Service, E., et al. (1997). Phonological short- verbal rehearsal speed in deaf children after cochlear implantation. Ear
term memory and new word learning in children. Dev Psychol, 33, 966–979. Hear, 24(Suppl 1), 106S–120S.
Geers, A. E., Moog, J. S., Biedenstein, J., et al. (2009). Spoken language Pisoni, D. B., & Geers, A. E. (2000). Working memory in deaf children with
scores of children using cochlear implants compared to hearing age- cochlear implants: Correlations between digit span and measures of spo-
mates at school entry. J Deaf Stud Deaf Educ, 14, 371–385. ken language processing. Ann Otol Rhinol Laryngol Suppl, 185, 92–93.
Geers, A. E., Nicholas, J., Tobey, E., et al. (2016). Persistent language delay Pisoni, D. B., Kronenberger, W. G., Chandramouli, S. H., et al. (2016).
versus late language emergence in children with early cochlear implanta- Learning and memory processes following cochlear implantation: The
tion. J Speech Lang Hear Res, 59, 155–170. missing piece of the puzzle. Front Psychol, 7, 493.
Hale, S., Rose, N. S., Myerson, J., et al. (2011). The structure of working Pisoni, D. B., Kronenberger, W. G., Roman, A. S., et al. (2011). Measures of
memory abilities across the adult life span. Psychol Aging, 26, 92–110. digit span and verbal rehearsal speed in deaf children after more than 10
Hall, M. L., Eigsti, I. M., Bortfeld, H., et al. (2018). Auditory access, language years of cochlear implantation. Ear Hear, 32(Suppl 1), 60S–74S.
access, and implicit sequence learning in deaf children. Dev Sci, 21, e12575. Poppen, R., Stark, J., Eisenson, J., et al. (1969). Visual sequencing perfor-
Harris, M. S., Kronenberger, W. G., Gao, S., et al. (2013). Verbal short-term mance of aphasic children. J Speech Hear Res, 12, 288–300.
memory development and spoken language outcomes in deaf children Svirsky, M. A., Teoh, S. W., Neuburger, H. (2004). Development of lan-
with cochlear implants. Ear Hear, 34, 179–192. guage and speech perception in congenitally, profoundly deaf children
Holden, L. K., Finley, C. C., Firszt, J. B., et al. (2013). Factors affecting as a function of age at cochlear implantation. Audiol Neurootol, 9,
open-set word recognition in adults with cochlear implants. Ear Hear, 224–233.
34, 342–360. Torkildsen, J. V. K., Arciuli, J., Haukedal, C. L., et al. (2018). Does a lack
Horn, D. L., Davis, R. A., Pisoni, D. B., et al. (2005). Development of visual of auditory experience affect sequential learning? Cognition, 170,
attention skills in prelingually deaf children who use cochlear implants. 123–129.
Ear Hear, 26, 389–408. Ulanet, P. G., Carson, C. M., Mellon, N. K., et al. (2014). Correlation
Ibertsson, T., Hansson, K., Asker-Àrnason, L., et al. (2009). Speech rec- of neurocognitive processing subtypes with language performance
ognition, working memory and conversation in children with cochlear in young children with cochlear implants. Cochlear Implants Int, 15,
implants. Deafness Educ Int, 11, 132–151. 230–240.
Khan, S., Edwards, L., Langdon, D. (2005). The cognition and behaviour van Boxtel, M. P., van Beijsterveldt, C. E., Houx, P. J., et al. (2000). Mild
of children with cochlear implants, children with hearing aids and their hearing impairment can reduce verbal memory performance in a healthy
hearing peers: A comparison. Audiol Neurootol, 10, 117–126. adult population. J Clin Exp Neuropsychol, 22, 147–154.

Copyright © 2018 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.
12 Davidson et al. / EAR & HEARING, VOL. XX, NO. XX, 00–00

Wass, M., Ibertsson, T., Lyxell, B., et al. (2008). Cognitive and linguistic Zekveld, A. A., Deijen, J. B., Goverts, S. T., et al. (2007). The relationship
skills in Swedish children with cochlear implants - Measures of accuracy between nonverbal cognitive functions and hearing loss. J Speech Lang
and latency as indicators of development. Scand J Psychol, 49, 559–576. Hear Res, 50, 74–82.
Watson, D. R., Titterington, J., Henry, A., et al. (2007). Auditory sensory
memory and working memory processes in children with normal hearing
and cochlear implants. Audiol Neurootol, 12, 65–76. REFERENCE NOTE
Wechsler, D. (2003). Wechsler Intelligence Scale for Children (4th ed.)
(WISC-IV). San Antonio, TX: Pearson. 1. Haskins, H. (1949). A Phonetically Balanced Test of Speech Discrimi-
Wyke, M. A., & Asso, D. (1979). Perception and memory for spatial relations nation for Children. Unpublished Master’s Thesis. Evanston, IL: North-
in children with developmental dysphasia. Neuropsychologia, 17, 231–239. western University.

Copyright © 2018 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.

You might also like