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Brain and Cognition 150 (2021) 105706

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Brain and Cognition


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Pragmatic abilities in early Parkinson’s disease


Maria Alice Baraldi a, *, Laura Avanzino b, c, Elisa Pelosin b, d, Filippo Domaneschi e,
Simona Di Paola f, Giovanna Lagravinese b, d
a
Department of Educational Sciences (DISFOR), Psychology Unit, Corso Podestà 2, University of Genoa, 16128 Genoa, Italy
b
IRCCS Policlinico San Martino, Largo Benzi 10, 16132 Genoa, Italy
c
Department of Experimental Medicine (DIMES), Section of Human Physiology, Via Leon Battista Alberti 2, University of Genoa, 16132 Genoa, Italy
d
Department of Neuroscience, Rehabilitation, Ophthalmology, Genetics and Maternal Child Health (DINOGMI), Largo Daneo 3, University of Genoa, 16132 Genoa, Italy
e
Laboratory of Language and Cognition, Via Balbi 30, University of Genoa, 16126 Genoa, Italy
f
Laboratory of Language and Cognition, Via Balbi 2, University of Genoa, 16126 Genoa, Italy

A R T I C L E I N F O A B S T R A C T

Keywords: Language impairment in Parkinson’s disease (PD) has been investigated at different levels of linguistic skills.
Parkinson’s disease Only a few studies dealt with pragmatic abilities in PD, and these suggest an impairment of pragmatic skills,
Pragmatics which might affect quality of life. However, previous studies enrolled patients with heterogeneous symptom
Executive functions
severity. The goal of this study is twofold: first, to investigate whether pragmatic skills are compromised at the
Theory of mind
Pragmatic disorders
early stage of PD; second, to explore whether an early pragmatic impairment is explained by a decay of a specific
Communication cognitive function. We assessed pragmatic abilities (discourse production, comprehension of narratives, humour,
and figurative language), and a cluster of cognitive functions (memory, verbal fluency, inhibition, shifting, and
ToM) in a sample of early PD patients and a group of age-matched healthy controls. Early PD patients showed
impaired general pragmatic skills (the ability to perform different pragmatic tasks in language production and
comprehension), as well as a deficit in the production and comprehension individual scores. Our results suggest
that good general cognitive skills (a good overall cognitive level) and high education support patients’ pragmatic
competence. Inhibitory processes have been found to predict patients’ ability to understand figurative language,
such as metaphors, and this might be related to frontal lobe dysfunctions.

1. Introduction evident condition of dementia (Papagno & Trojano, 2018). To date, the
impairment of executive functions has been well documented in patients
Parkinson’s disease (PD) is a chronic, neurodegenerative disorder, with PD, and it typically encompasses several domains, such as plan­
whose pathophysiology is characterized by the loss of dopaminergic ning, set-shifting, working memory, inhibition, decision making, dual
neurons in the substantia nigra pars compacta causing a dopaminergic task performance, and cognitive control (McKinlay, Grace, Dalrymple-
deficiency in the basal ganglia circuitry. The clinical diagnosis is still Alford, & Roger, 2010; Papagno & Trojano, 2018). Executive dysfunc­
mainly based on United Kingdom Parkinson’s Disease Society Brain tions have been associated with the dopamine depletion in the striatum,
Bank clinical diagnostic criteria (UKPDSBB- Hughes et al., 1992). PD is which leads to a disruption of the frontal-striatal circuitry (Papagno &
an extremely heterogeneous disorder, which is defined by the presence Trojano, 2018). The strong connectivity of the basal ganglia with
of motor features including muscle rigidity, bradykinesia, resting cortical – mainly frontal and limbic – areas may also explain the
tremor, and postural instability (e.g., Morgan & Fox, 2016; Poewe et al., vulnerability of many functions related to language and non-verbal
2017). However, several non-motor features have been reported as well, communication in patients with PD (Papagno & Trojano, 2018; Pell &
such as mood alterations, sleeping problems and cognitive changes (e.g., Monetta, 2008). With regard to verbal language, the available literature
Caballol, Martí, & Tolosa, 2007; Menza, Dobkin, Marin, & Bienfait, suggests that PD patients show an impairment, especially in language
2010; Robbins & Cools, 2014). Cognitive symptoms may be from mild, production, at the semantic and (morpho-)syntactic level (Holtgraves &
which do not affect everyday life, to severe, leading to a clinically Giordano, 2017). Only a few studies addressed specific pragmatic skills

* Corresponding author at: University of Genoa, Department of Educational Sciences (DISFOR), Psychology Unit, Corso Andrea Podestà 2, 16128 Genoa, Italy.
E-mail addresses: mariaalice.baraldi@edu.unige.it (M.A. Baraldi), laura.avanzino@unige.it (L. Avanzino), elisa.pelosin@unige.it (E. Pelosin), filippo.
domaneschi@unige.it (F. Domaneschi), simona.dipaola@edu.unige.it (S. Di Paola), giovannalagravinese@yahoo.it (G. Lagravinese).

https://doi.org/10.1016/j.bandc.2021.105706
Received 18 September 2020; Received in revised form 8 February 2021; Accepted 9 February 2021
Available online 21 March 2021
0278-2626/© 2021 Elsevier Inc. All rights reserved.
M.A. Baraldi et al. Brain and Cognition 150 (2021) 105706

in patients with PD, and these suggested that some pragmatic abilities, has been also devoted to cognitive functions and, more specifically, to
such as turn-taking, might be compromised in this clinical population the possible relation between executive functions (i.e., a cluster of
(McNamara & Durso, 2003). Pragmatic skills refer to the ability to use cognitive processes involved in goal-directed actions) and pragmatic
language in context (Grice, 1975; Levinson, 1983). The crucial role of processing. Thus, it is possible to conclude that pragmatic abilities might
pragmatic abilities is evident whenever the recognition of the speaker’s rely on ToM but also, sometimes more prominently, on clusters of
intended meaning is required, i.e., what a speaker means to communi­ cognitive functions (Martin & McDonald, 2003).
cate by uttering a sentence in a context. Examples of pragmatic phe­
nomena are metaphors, irony and other forms of non-literal language 2. Pragmatic abilities in Parkinson’s disease
but also presuppositions, implicatures, context sensitivity and deixis,
comprehension of explicit and implicit contents in narratives, and other Only a few studies investigated pragmatic abilities in PD and these
phenomena at the discourse level, like topic maintenance and coher­ found that individuals with PD display both language comprehension
ence, information flow, politeness, the ability to respect turn-taking and production deficits (Holtgraves & Cadle, 2016), thus suggesting that
rules, to communicate appropriate amount of information, to begin pragmatic skills might be impaired.
and end a conversation, to make socially appropriate requests and to
provide thematically cohesive narratives of relevant events (McNamara 2.1. Pragmatic production and comprehension
& Durso, 2003). Moreover, several researches also investigated other
non-verbal domains, such as intonation, eye-contact, facial expressions, As for pragmatic production, several researches reported deficits for
gestures and proxemics, since they all contribute to an effective and both verbal (conversational initiation, turn taking, topic maintenance,
goal-oriented communication (Holtgraves & Cadle, 2016). response length and referencing skills) and non-verbal (intonation, eye-
Clinical pragmatics is a field of pragmatic research which explores contact, facial expressions, gestures, and proxemics) dimensions (Hall,
the characterization, assessment and treatment of pragmatic disorders Ouyang, Lonnquist, & Newcombe, 2011; Holtgraves & Cadle, 2016;
across the lifespan (Cummings, 2017). This research field has been a Holtgraves, Fogle, & Marsh, 2013). Holtgraves and colleagues (2013)
major growing area in linguistics over the past two decades, since a showed that patients with PD produce significantly more under­
significant number of patients with impaired language skills also show informative sentences as compared to healthy participants. Further­
deficits in the pragmatic domain. As suggested by researches in clinical more, PD patients exhibited worse production skills in tasks targeting
pragmatics, these communicative skills might be impaired in several discourse organization, engagement in conversation, and the ability to
populations. Although the available studies focus mainly on atypical produce informative descriptions of different pictures (Montemurro
development (Eales, 1993; Green, Johnson, & Bretherton, 2014; Mur­ et al., 2019). In addition, it has been argued that patients with PD tend to
phy, Faulkner, & Farley, 2014), there is considerable research targeting produce not only syntactically simple language, but also abnormalities
aging (Mak & Carpenter, 2007; Messer, 2015; Shammi & Stuss, 2003; in speech fluency such as prolonged and inappropriate pauses (Holt­
Uekermann, Thoma, & Daum, 2008) and different clinical conditions, graves & Cadle, 2016). Lastly, it has been suggested that production
such as schizophrenia (Bambini et al., 2016; Bosco, Gabbatore, Gastaldo, deficits might be linked to the severity of motor symptoms (Holtgraves &
& Sacco, 2016; Haas et al., 2015; Parola, Berardinelli, & Bosco, 2018), Cadle, 2016). In particular, Illes, Metter, Hanson, and Iritani (1988)
traumatic brain injuries (Angeleri et al., 2008; Bosco et al., 2017, 2015; found that PDs’ syntactically simple sentences may reflect a compen­
Douglas, 2010), as well as neurological disorders. In fact, a disruption of satory mechanism to reduce speech-motor difficulties.
pragmatic abilities has also been observed in patients with Alzheimer’s As for pragmatic comprehension, this seems compromised too in PD
disease (Amanzio, Geminiani, Leotta, & Cappa, 2008; Feyereisen, Ber­ (Cummings, 2017), especially the understanding of figurative language,
rewaerts, & Hupet, 2007; Luzzi et al., 2020; Rapp & Wild, 2011), verbal irony and other implicit contents (Lewis, Lapointe, Murdoch, &
Amyotrophic Lateral Sclerosis (Bambini et al., 2016, 2020; Fisher, Chenery, 1998; Monetta, Grindrod, & Pell, 2009; Papagno & Trojano,
Philpott, Andrews, Maule, & Douglas, 2017), as well as precisely PD 2018; Pell & Monetta, 2008). For example, in Berg, Björnram, Hartelius,
(McNamara & Durso, 2003; Monetta & Pell, 2007; Montemurro et al., Laakso, and Johnels (2003), PD patients exhibited difficulties in making
2019). These communication deficits lead to difficulties in interacting inferences, understanding metaphors and lexical ambiguities (Berg
with others and in engaging in social relationships, with a consequent et al., 2003). Additionally, Thaler et al. (2012) showed that PD patients
worsening of patients’ quality of life (Joyal, Bonneau, & Fecteau, 2016; have a significantly poorer sense of humour than control participants
Tan, Thomas, & Rossell, 2014). (Thaler et al., 2012). In a story comprehension paradigm, Murray and
Many studies shed light on the underlying mechanisms of pragmatic Stout (1999) tested PD patients’ ability to identify the main ideas of a
processing. Deriving the speaker’s intended meaning has been tradi­ story versus details of the story, as well as their ability to comprehend
tionally linked to the ability of attributing mental states to others, an explicit versus implied information (Murray & Stout, 1999). Patients
inferential mechanism that is commonly referred to as Theory of Mind – were more accurate on questions about the main ideas as compared to
ToM (Brüne & Bodenstein, 2005; Sperber & Wilson, 2002). Despite questions about the story details; moreover, they were more accurate in
pragmatics has been previously considered as a submodule of mind- identifying explicit than implied information. In addition, Montemurro
reading (Sperber & Wilson, 2002), there is growing evidence showing et al. (2019) tested PD patients’ and healthy controls’ ability to under­
that pragmatic competence is a more complex phenomenon, which stand a set of pragmatic phenomena such as narrative, humour and
cannot be limited to the ability to understand others’ mental states and figurative language, and found that PD patients scored lower in both the
intentions (Bosco, Tirassa, & Gabbatore, 2018). With respect to this narrative and humour comprehension tasks.
premise, it is not possible to conclude that pragmatic abilities rely on
ToM only (Domaneschi & Bambini, 2020)1. To date, growing interest 2.2. Pragmatic abilities and cognitive functions

To date, some studies showed that changes in pragmatic abilities (in


1 both the production and comprehension modalities) are often related to
This latest view is supported by recent findings showing that ToM alone
concomitant cognitive deficits (Colman & Bastiaanse, 2011; McNamara
cannot explain the performance of children (Bosco & Gabbatore, 2017a, 2017b)
and patients with schizophrenia (Bosco et al., 2012) in different pragmatic & Durso, 2003; Monetta & Pell, 2007). McNamara and Durso (2003)
tasks. Furthermore, another reason to rule out the thesis of an overlap of ToM found a correlation between PD patients’ compromised turn-taking
and pragmatics lies in the neural substrates and in the developmental and decay abilities and disrupted frontal-lobe functioning (McNamara & Durso,
patterns of pragmatic competence, which are distinct from ToM (Domaneschi & 2003). Furthermore, Holtgraves and colleagues (2013) assessed pa­
Bambini, 2020). tients’ ability to comprehend and produce informative utterances and

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showed that this is related to executive control deficits (Holtgraves et al., motor area, as well as dorsal and ventral regions of the frontal cortex,
2013). In Monetta and Pell (2007), PD patients with impaired working which are particularly engaged during cognitive tasks (Middleton &
memory were also significantly slower and less accurate than healthy Strick, 2000a, 2000b). Some authors suggested that two specific regions
controls in processing metaphors, and similar findings have been shown are considered of particular interest for cognitive decline in PD: (i) the
in a follow up study on pragmatic inference generation (Monetta, orbito-frontal cortex (OFC), which is associated with decision making,
Grindrod, & Pell, 2008) and irony comprehension (Monetta et al., and (ii) the anterior cingulate cortex (ACC), which supports conflict
2009). Furthermore, McKinlay, Dalrymple-Alford, Grace, and Roger monitoring, response initiation and inhibition (Palermo et al., 2017). It
(2009) suggested that processing speed strongly influences PD patients’ is possible to argue that deficits of executive functions in PD progress
pragmatic performance on a set of tasks that involved the ability to (i) with motor disabilities, and pragmatic decline is strictly related to these
recognize lexical and structural ambiguities of a sentence, (ii) make cognitive changes. For example, a study by Monetta and Pell (2007)
inferences, (iii) formulate appropriate sentences for a given situation, showed that PD patients are less efficient in the processing of metaphors,
and (iv) interpret metaphorical expressions (McKinlay et al., 2009). and this difficulty is related to reduced working memory (WM) capacity,
Finally, there is considerable research targeting ToM in PD. The which engages activity of the prefrontal cortex (Monetta & Pell, 2007).
available findings suggest that ToM difficulties often occur in this clin­ Consistently, McNamara and Durso (2003) found that impaired prag­
ical population (e.g., Bodden et al., 2010; Freedman & Stuss, 2011; matic skills in PD (conversational appropriateness, speech acts, stylis­
Poletti, Enrici, Bonuccelli, & Adenzato, 2011), in both the cognitive and tics, gestures, and prosodics) were related to measures of frontal lobe
affective components (Bodden et al., 2010; Raffo De Ferrari et al., 2015), functioning (i.e., the Stroop test, the Tower of London, and the Design
although the impairment of cognitive ToM might only arise in the late Fluency task) (McNamara & Durso, 2003), in line with other evidence
course of the illness (Péron et al., 2009). As for the role of ToM in suggesting that PD patients perform abnormally on tests measuring
pragmatic abilities in PD, research is still very limited. To the best of our planning (such as the Tower of London) and inhibition (such as the
knowledge, one of the few available studies is Vachon-Joannette, Stroop test) (Weintraub et al., 2005). In sum, it is possible to conclude
Tremblay, Langlois, Chantal, and Monetta (2013) that reported signifi­ that the neural bases of pragmatic competence in PD still need to be
cant correlations between PD patients’ metaphor comprehension and clarified. However, frontal lobe deficits might be responsible for the
ToM abilities (Vachon-Joannette et al., 2013). observed difficulties in pragmatic language processing.

2.3. Neural underpinnings of pragmatic skills in Parkinson’s disease 2.4. Aims of the study

The classical brain structures associated with language include the To date, little is known about pragmatic abilities in patients with PD.
Broca’s area in the left inferior frontal gyrus (IFG), the Wernicke’s area The few available studies report an impairment in pragmatic produc­
in the left superior temporal gyrus (STG), as well as parts of the left tion, which seems to be linked to motor disabilities as well as cognitive
middle temporal (MTG) and angular gyrus (Friederici, 2011). Several deficits. Pragmatic comprehension seems compromised as well, and the
studies suggested a different role of the two hemispheres; while the left impairment seems to stem from patients’ cognitive dysfunction. Yet, to
hemisphere seems to support the processing of close semantic relation­ date, a wealth of open issues cries out for further investigation.
ships, the right hemisphere is more involved in the analysis of distant First, most of the available studies enrolled PD patients whose
semantic concepts, as in the case of figurative language (Jung-Beeman, symptom severity was highly heterogeneous, thus not focusing on a
2005; Rapp, Mutschler, & Erb, 2012). However, pragmatics is consid­ specific stage of the disease (McKinlay, Dalrymple-Alford, Grace, &
ered a complex linguistic phenomenon resulting from the interplay of Roger, 2009; Montemurro et al., 2019). Crucially, a clear and complete
social and cognitive skills (Van Lier et al., 2016) and, for this reason, it is picture of pragmatic impairment in early PD patients is missing, as it is
not possible to reduce its neural functioning to a single brain area or to still uncertain if and how these skills are compromised at this stage. To
the activity of the right hemisphere only. To date, less is known of the the best of our knowledge, Montemurro and colleagues (2019) is the
neural structures underlying pragmatic competence in patients with PD. only study that targeted pragmatic abilities through a comprehensive
The existing literature suggests that two major language networks are assessment; however, the group of PD patients was not balanced in terms
modulated by the dopamine circuits: the frontal-parietal network (FPN), of the severity of the disease. In fact, the heterogeneity of the sample
which mediates grammatical/syntactic aspects of language, and the so- does not allow to clearly characterize the onset of the pragmatic deficit.
called social brain network, which supports pragmatic processing An early identification of pragmatic impairment is essential for at least
(McNamara & Durso, 2018). The social brain network is made of a set of two main reasons. On the one hand, it is crucial to understand if and to
areas involved in social tasks such as inferring intentions, emotions and what extent pragmatic abilities are impaired in the early-course of the
beliefs of others, including: (i) the ventral striatum, (ii) the limbic areas, disease. On the other hand, this would allow monitoring the progression
(iii) the fusiform gyrus, (iv) the ventromedial and dorsomedial pre­ of the impairment over time. Importantly, patients’ quality of life, which
frontal cortex, (v) the frontopolar area, (vi) the superior and medial slowly worsens due to motor impairments, is also affected by the ability
temporal sulcus, (vii) the temporo-parietal junction (TPJ), (viii) the to successfully communicate with others. Deficits in both pragmatic
insula and the precuneus (Adolphs, 2009; Dunbar, 2012; McNamara & comprehension and production will likely cause communication diffi­
Durso, 2018). PD patients show deficits at both linguistic levels, as well culties. In turn, patients will experience reduced socialization.
as dysfunctions of both brain networks. However, due to the observed Second, despite some authors suggested that the impairment of
difficulties in pragmatic competence, McNamara and Durso (2018) pragmatic abilities in PD might be due to a cognitive dysfunction, the
suggested that the impairment of the social brain network is more severe existing evidence about this link is still conflicting. Interestingly, Mon­
in patients with PD (McNamara & Durso, 2018). Furthermore, the few temurro et al., 2019 found that Cognitive Reserve (i.e., the resilience to
existing evidence on the neural underpinnings of pragmatic skills con­ cognitive deficit, which is determined by life experiences and cognitive
cerns the relationship between pragmatic competence and executive activity, such as years of education, number of intellectually stimulating
functions, which are typically supported by frontal brain areas. In fact, leisure activities, degree of occupational complexity, quality of social
there is substantial neuropsychological evidence showing frontal defi­ interactions, etc.) might have a compensatory effect on the decline of
cits in PD, as many patients perform poorly on neuropsychological tests pragmatic abilities. This is interesting because it opens to the possibility
traditionally linked to frontal lobe functions (Gotham, Brown, & Mars­ that cognitive (dys)function might play a role in the pragmatic impair­
den, 1988; Taylor & Saintcyr, 1995). Interestingly, the frontal areas are ment in PD. Crucially, in order to investigate the relationship between
one of the targets of the basal ganglia outflow. Projections from the pragmatic competence and cognitive skills, a comprehensive neuro­
striatum are directed to premotor regions, such as the supplementary psychological assessment including both screening batteries (i.e., brief

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tests covering several cognitive domains - e.g., orientation, memory, Table 1


language, executive functions etc., administered to detect cognitive Demographic and Clinical variables of patients with early PD. The first column
impairment and the overall cognitive level), and domain-specific tests (i. reports the ID, the second the Age (number of years), the third the Education
e., tools for the assessment of a specific cognitive function - e.g., working (number of years), the fourth the Sex (Female or Male), the fifth the Years from
memory, shifting, inhibitory control, etc.) would be needed. Onset, the sixth the disease severity (Hoehn and Yahr score -H&Y), and the
seventh the motor examination (Unified Parkinson Disease Rating Scale score
The present study has two main goals. First, to trace a comprehensive
-MDS UPDRS-III).
characterization of pragmatic abilities in early PD patients. Second, to
investigate whether a pragmatic impairment in early PD might stem ID Age Education Sex Years Disease Motor
from severity examination
from emerging deficits of specific cognitive functions. No studies have
Onset (H&Y) (MDS UPDRS
been previously conducted in this respect, and this prevents us from III)
developing specific predictions. However, cognitive functions are
PD_01 84 15 M 3 2 28
notably compromised in PD. If cognitive deficit is already visible at an PD_02 69 13 M 3 2 12
early stage of the disease, then we expect to observe an early pragmatic PD_03 70 8 M 4 1.5 8
impairment in those pragmatic phenomena whose processing relies PD_04 65 13 M 4 2 16
more on faculties such as attention, inhibition, and working memory. PD_05 76 8 M 6 2 15.5
PD_06 69 17 M 8 2 32
PD_07 72 8 F 3 1.5 16
3. Materials and method PD_08 72 13 F 3 2 23.5
PD_09 68 13 M 2 2 17
3.1. Participants PD_10 70 13 M 7 1.5 11
PD_11 62 16 F 7 2 12.5
PD_12 71 8 F 10 2 27
Eighteen early PD patients [mean age 69.77(5.87); mean years of PD_13 65 8 M 3 2 20
education 11.38(3.39); mean Hoehn&Yahr 1.88(0.21); 4 F, 14 M] were PD_14 75 13 M 5 2 12
recruited at the IRCCS San Martino Hospital (Genova, Italy). PD is a PD_15 78 5 M 3 1.5 10
progressive neurological disorder defined by a characteristic clinical PD_16 65 13 M 3 2 23
PD_17 63 13 M 10 2 17
syndrome, bradykinesia plus rest tremor or rigidity (Postuma et al.,
PD_18 62 8 M 6 2 31
2015). There are a large number of different disorders that can have
some or all of these clinical features, and the clinical syndrome is
referred to as “parkinsonism.” We excluded patients affected by and university/college courses successfully completed, duration of
parkinsonism such as progressive supranuclear palsy (PSP), multiple illness for the PD group, quantified as number of years from onset); (ii)
system atrophy (MSA) or Lewy body dementia (LBD), which have a the APACS test, Assessment of Pragmatic Abilities and Cognitive Substrates
different pathologic substrate respect to PD. The clinical evaluation of (Arcara & Bambini, 2016), to collect measures for their pragmatic
patients’ PD stage was conducted according to the following procedure: competence; (iii) a battery of selected neuropsychological tests that
disease severity was evaluated with the Hoehn and Yahr (H&Y; “Par­ included both screening tests (brief tools assessing general cognitive
kinson’s Disease: Hoehn and Yahr Scale,” 2012) and with Movement functioning), and domain-specific tests (tools for the assessment of
Disorders Society (MDS) - Unified Parkinson’s Disease Rating Scale specific cognitive functions).
(UPDRS) part III (MDS UPDRS-III -motor examination) (Goetz et al.,
2008). The H&Y scale assesses the severity of the disease based on 3.2.1. Pragmatic assessment
bilateral motor involvement, and the impairment of gait and balance. Following Montemurro et al., 2019, participants were assessed for
The original 5-point scale (stage 1–5) was subsequently modified to a 7- their pragmatic abilities with the Assessment of Pragmatic Abilities and
point scale, including stages 1.5 and 2.5. MDS UPDRS-III is a motor Cognitive Substrates (APACS; Arcara & Bambini, 2016), a standardized
examination evaluating aspects such as speech, facial expressions, ri­ measure assessing both discourse production and comprehension by
gidity, hand movement, leg agility, gait, postural stability, bradykinesia, means of six tasks.
and tremor at rest. The inclusion criteria were: (1) idiopathic PD diag­ The APACS test consists of two sections: the first one assesses Prag­
nosis; (2) HY scale score between 1.0 and 2.0 (bilateral, mild-symptoms matic Production and is composed of two dedicated tasks; the second
with recovery on pull test); (3) stable medication use; (4) Montreal one evaluates Pragmatic Comprehension and is composed of four
Cognitive Assessment score > 15.5 (Santangelo et al., 2015); (6) no dedicated tasks. Three main composite scores are computed: a com­
audiometric deficits; (7) no other neurological disease history. Data of posite score for production, one for comprehension and a composite
PD patients together with some relevant clinical information are re­ score for participants’ overall performance in APACS (i.e., APACS
ported in Table 1. Total). In what follows, we now describe each task in each of the two
A sample of 21 healthy controls matched with the PD group [mean sections, as well as the scoring procedure.
age 70.42(3.77); mean years of education 13.19(3.85); 12 F, 9 M] was Task 1: Interview (production). It is a semi-structured interview based
recruited from the Creative Mind Cafè, an elderly community centre on autobiographical topics that assesses discourse organization and
located in Genoa. engagement in conversation. It evaluates several dimensions of
All participants were Italian native speakers, and they were tested in discourse, such as speech (e.g., repetition, echolalia, incomplete utter­
a quiet room at the Department of Neuroscience (University of Genoa). ances), informativeness (over- or under-informativeness), information
This study was approved by the local Ethical Committee and was flow (missing referents, wrong order of the discourse elements, topic
carried out in agreement with legal requirements and international shift), and paralinguistic aspects (altered intonation, fixed facial
norms (Declaration of Helsinki, 1964). Written informed consent was expression, abuse of gestures, loss of eye-contact). For each type of
obtained from every participant prior to the beginning of the communication deficit, the frequency of occurrence is collected (i.e.,
experiment. always/sometimes/never) and the correspondent score is assigned (i.e.,
0/1/2). The maximal score is 44.
3.2. Materials and procedure Task 2: Description (production). This task measures the ability to
produce informative descriptions of 10 pictures that depict scenes of
Participants were administered a set of measures, in the following everyday life. Participants’ production of salient elements for each
order: (i) a survey that collected relevant demographic and clinical in­ picture is coded and this is scored as 0/1/2, with 0 indicating a missed
formation (age and education, quantified as number of years of school identification, 1 a partially correct identification, and 2 a good

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identification. The maximal score for is 48. recall verbal memory, confrontation naming test, sustained attention,
Task 3: Narratives (comprehension). Participants are read six stories working memory, unprompted drawing of a clock, copy drawing of a
inspired by real newspapers. Each story is followed by: (i) one open clock, delayed free-recall verbal memory, alternate verbal fluency and
question about the global topic of the story; (ii) 2-to-4 yes-no compre­ action verbal fluency. Three scores are obtained (subcortical, cortical
hension questions on explicit and implicit contents rated 1 when and Total). See Appendix for details.
correctly answered, or 0 when incorrectly answered; (iii) 2 questions
that elicit a verbal explanation of the 2 figurative expressions embedded 3.2.2.2. Domain specific measures
in the story. Participants’ answers to (i) are coded as 2 when the global 3.2.2.2.1. Memory. Digit Span forward (Monaco, Costa, Caltagirone,
topic is correctly identified, 1 when a partially correct identification of & Carlesimo, 2013; Orsini et al., 1987). This measures short-term verbal
the global topic is provided, or 0 when the topic is not correctly iden­ memory. See Appendix for details.
tified. Participants’ answers to (iii) are rated 2 if a good explanation is Corsi Span forward (Monaco et al., 2013; Spinnler & Tognoni, 1987).
provided, 1 if participants provide an incomplete explanation or an This test measures short-term visuo-spatial memory. See Appendix for
example, or 0 if participants provide a literal explanation, a paraphrase details.
or no explanation at all. The maximal score for is 56. “Valutazione delle capacità di costruzione dello scheletro” (Semantic
Task 4: Figurative language 1 (comprehension). This task provides a Memory 1 test) and“Denominazione visiva” (Semantic Memory 2 test)
measure for the ability to infer non-literal meanings. Participants are (Sartori & Job, 1988). These tests measure semantic memory. See Ap­
first presented with idioms, novel metaphors and proverbs and they are pendix for details.
asked multiple-choice questions for each item. Participants’ accuracy is 3.2.2.2.2. Executive functions. Digit Span backward (Monaco et al.,
collected and coded as 0 or 1, depending on (in)correct response se­ 2013). This test measures verbal working memory. See Appendix for
lection. The maximal score is 15. details.
Task 5: Humor (comprehension). The subtest measures the ability to Corsi Span backward (Monaco et al., 2013). This tests evaluates visuo-
comprehend verbal humor through a multiple-choice task. Participants spatial working memory. See Appendix for details.
are asked to pick the best punch line of a story. Accuracy is collected and Verbal fluency test (Novelli, Papagno, Capitani, Laiacona, Vallar, &
scored as 0/1. The maximal score is 7. Cappa, 1986). This test assesses both semantic and phonemic fluency.
Task 6: Figurative language 2 (comprehension). This is a second, more See Appendix for details.
direct, measure for the ability to infer non-literal meanings. Participants Trail Making Test (TMT) (Mondini, Mapelli, Vestri, & Bisiacchi,
are asked to explain the meaning of 15 figurative expressions (i.e., id­ 2003). This assesses set-shifting. See Appendix for details.
ioms, novel metaphors and proverbs) and their accuracy is collected. For Stroop test (short version) (Caffarra, Vezzadini, Dieci, Zonato, &
each expression, the participants’ explanation is scored 2 if a good Venneri, 2002; Venneri et al., 1992). This test measures inhibition and
description of the meaning of the figurative expression is provided, 1 if cognitive control. See Appendix for details.
an incomplete explanation or an appropriate example is provided, or 0 if 3.2.2.2.3. Theory of Mind. Emotion Attribution Test (EAT) (Blair,
a literal explanation or a paraphrase is provided, or participants don’t 2000; Prior, Marchi, & Sartori, 2003) and Reading the Mind in the Eyes test
know the meaning of the expressions. The maximal total score is 30. (RMEt) (Baron-Cohen, Wheelwright, Hill, Raste, & Plumb, 2001). These
Composite scores and cut-off values. The Pragmatic Production com­ tests both measure affective ToM. See Appendix for details.
posite score is obtained from the average of the sub-scores in Interview Advanced ToM test (Blair, 2000; Happé, 1994; Prior et al., 2003). This
and Description, which are first transformed in proportion. The Prag­ assesses double bluff, white lies and persuasion. See Appendix for
matic Comprehension composited score is computed from the average of details.
the sub-scores in Narratives, Figurative Language 1, Figurative Language 2, 3.2.2.2.4. Depression. Beck Depression Inventory II (BDI-II) (Beck,
and Humour, transformed in proportion. The APACS Total score is the Steer, & Brown, 1996). It is a 21-item self-report inventory designed to
average of the Pragmatic Production and Pragmatic Comprehension assess the presence and severity of depressive symptoms. See Appendix
composite scores. In addition, PD patients’ scores in each task are for details.
compared to cut-off values in order to identify any impaired pragmatic
performance. 3.2.3. Procedure
Participants were tested individually in two experimental sessions
3.2.2. Cognitive assessment lasting about 1-hour each, which could allow us to collect a consistent
Given the exploratory nature of the study, a wide set of neuropsy­ amount of experimental measures without burdening the participants
chological tests has been administered. The selection of cognitive mea­ too much. The first session consisted of: (i) Assessment of Pragmatic
sures is consistent with the existing literature investigating the Abilities and Cognitive Substrates (APACS -Arcara & Bambini, 2016),
relationship between pragmatic abilities and cognitive skills. In fact, (ii) Digit Span (forward and backward -Monaco et al., 2013), (iii) verbal
general cognitive functioning, inhibition, working memory, verbal fluency test (Novelli et al., 1986), (iv) Corsi Span (forward and back­
fluency, set shifting, semantic memory, and ToM have been assessed in ward -Monaco et al., 2013), (v) Stroop test (Caffarra et al., 2002), (vi)
previous studies, and often linked to pragmatic processing (McKinlay, Trial Making Test (TMT -Mondini et al., 2003) and (vii) Reading the
Dalrymple-Alford, Grace, & Roger, 2009; Monetta & Pell, 2007; Mon­ Mind in the Eyes test (RMEt -Baron-Cohen et al., 2001)The second ses­
temurro et al., 2019; Yang, Fuller, Khodaparast, & Krawczyk, 2010). sion included: (i) Parkinson’s Disease-Cognitive Rating Scale (PD-CRS
Additionally, it is crucial to evaluate the depression status in both -Santangelo et al., 2014), (ii) Montreal Cognitive Assessment (MoCA
groups, since late-life depression might affect cognitive performance -Nasreddine et al., 2005), (iii) Advanced ToM test (Happé, 1994), (iv)
(Crocco, Castro, & Loewenstein, 2010). Emotion Attribution Test (Prior et al., 2003), (v) Semantic Memory 1
test (Sartori & Job, 1988), (vi) Semantic Memory 2 test (Sartori & Job,
3.2.2.1. Screening tests. Montreal Cognitive Assessment (MoCA) (Nas­ 1988), (vii) Beck Depression Inventory-II (BDI-II -Beck et al., 1996). The
reddine et al., 2005). This is a neuropsychological scale consisting of 8 tests were administered in fixed order, a common practice in research on
subtests that assess: memory, language, visuo-spatial skills, executive clinical populations and on individual differences to control for fatigue
functions, time and space orientation. See Appendix for details. and transfer effects across participants (Cavallini, Lecce, Bottiroli, Pal­
Parkinson’s Disease-Cognitive Rating Scale (PD-CRS) (Santangelo, ladino, & Pagnin, 2013; Lecce et al., 2019). The specific order was
Barone, Abbruzzese, Ferini-Strambi, & Antonini, 2014). This neuro­ constructed so as to give priority to the APACS test, which was the main
psychological scale consists of 9 subtests that assess: immediate free- measure of the study, and to maximally reduce the difficulty and

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cognitive fatigue between sessions as well as across tasks in each session. Table 2A
The table shows the results of the Wilcoxon-rank sum test comparing PD and
4. Data analysis controls on the APACS task, and on the APACS composite scores. The first col­
umn reports the name of the single tasks and the composite scores. The second
and third columns report the mean and SD of patients and healthy controls. The
First, group differences on APACS as well as on participants’ scores in
fourth column reports the Wilcoxon-rank sum test values and the fifth column
the battery of neuropsychological tests were analysed using the Wil­
reports the p-values. Asterisks indicate significant differences between groups:
coxon Rank Sum Test. As for APACS, this analysis was conducted on
** p < 0.01, * p < 0.05.
each of the subtasks (Interview, Description, Narratives, Figurative
APACS task or Mean Mean W p
Language 1, Humor, and Figurative Language 2) as well as on each of the
composite score Parkinson (SD) Controls (SD)
three composite scores (Pragmatic Production, Pragmatic Comprehen­
sion and APACS Total). Group differences were analysed for each of the Interview 39.55 (2.61) 42.52 (1.20) 334.5 <0.001**
Description 42.11 (3.62) 42.66 (4.19) 218 0.41
neuropsychological tests, as well as for ToM and depression measures. Narratives 45.66 (7.57) 49.38 (5.31) 240 0.14
We also analysed individual performance by (i) comparing each par­ Figurative Language 1 14.11 (0.90) 14.47 (0.81) 236.5 0.14
ticipant’s scores in APACS to the cut-off values (see Arcara & Bambini, Humour 6.27 (1.12) 6.28 (1.10) 190 0.97
2016), and (ii) adjusting raw scores of neuropsychological tests ac­ Figurative Language 2 20.55 (3.56) 23.80 (2.97) 293 0.003**
Pragmatic Production 0.88 (0.06) 0.92 (0.05) 277 0.013*
cording to age and education, and then converting adjusted scores into
Pragmatic 0.83 (0.09) 0.88 (0.07) 265 0.032*
five-point ordinal scale of Equivalent Scores (ES: 0 = scores equal or Comprehension
lower than the outer tolerance limit − 5%; 4 = scores higher than the APACS Total 0.86 (0.05) 0.90 (0.05) 290 0.004**
median value of the whole sample; 1, 2 and 3, obtained by dividing into
three equal parts the area of distribution between 0 and 4, Spinnler &
Tognoni, 1987). ToM and depression scores were also compared to cut- score (p = 0.004), Pragmatic Production (p = 0.013), Pragmatic
off values. Comprehension (p = 0.032), the Interview (p < 0.001) and Figurative
Second, for each of the two groups of participants, pairwise Pearson’s Language 2 (p = 0.003) tasks. No significant differences emerged be­
correlations were conducted to assess the relationship between partici­ tween patients and healthy elders in the Description, Narratives, Figu­
pants’ scores in each of the APACS tasks (i.e., Interview, Description, rative Language 1 and Humor tasks.
Narratives, Figurative Language 1, Humor, and Figurative Language 2,
Pragmatic Production, Pragmatic Comprehension and APACS Total) and 5.1.2. Neuropsychological measures
their performance in each of the cognitive measures as well as in the Table 2B reports the descriptive statistics and the details of the
ToM measures.
Third, a stepwise multiple regression analysis was performed sepa­
Table 2B
rately for PD patients and healthy controls to investigate which – if any –
The table shows the results of the Wilcoxon-rank sum test comparing PD and
of the collected cognitive measures significantly predicts pragmatic
controls on all of the administered cognitive tests. The first column reports the
performance. Given the high number of cognitive variables, for the sake name of the test, task or scale. The second and third columns report the mean
of the statistical models, we first selected the predictors based on their and SD of patients and healthy controls. The fourth column reports the
significant correlation with the APACS measures. Starting from this Wilcoxon-rank sum test values and the fifth column reports the p-values. As­
procedure, some of the selected cognitive variables have been excluded terisks indicate significant differences between groups: ** p < 0.01, * p < 0.05.
later to prevent the models to be affected by multicollinearity. The final Neuropsychological Mean Mean W p
models included the following predictors: age, education, sex, MDS Measures Parkinson Controls
UPDRS-III (a measure of the degree of motor symptoms, for the PD group (SD) (SD)
only), the Stroop performance (both the time and the error interference Digit Span_forward 5.57 (0.95) 6.35 (1.19) 242.5 0.13
effects), and the PD-CRS (the cognitive scale for PD) Total score. This Digit Span_backward 4.44 (0.82) 4.83 (0.80) 231 0.23
selection is also consistent with the existing literature on pragmatic Phonemic fluency 38.05 (10.97) 40.47 (9.70) 199.5 0.76
Semantic fluency 47.00 (7.85) 48.95 (8.45) 208.5 0.37
abilities. In fact, the severity of motor symptoms, a general measure of
Corsi_forward 4.70 (0.95) 4.76 (0.96) 175 0.91
cognitive skills, inhibition, cognitive control and other relevant de­ Corsi_backward 4.34 (1.13) 5.13 (0.71) 264 0.011*
mographic variables have been previously linked to pragmatic skills in Stroop_accuracy 0.85 (2.51) 0.19 (0.56) 206.5 0.33
patients with PD (Colman & Bastiaanse, 2011; Holtgraves et al., 2013). Stroop_time 27.66 (17.73) 18.45 (8.33) 112 0.05*
Given the exploratory nature of these analyses and the absence of pre­ TMT 38.95 (30.09) 20.13 118 0.045*
(22.44)
vious experimental evidence on the same topic, a backward method
MoCA_Total 26.68 (2.55) 25.28 (2.62) 110.5 0.13
based on Akaike Information Criterion (AIC) values was applied to PDCRS_immediate verbal 8.94 (1.93) 9.67 (1.59) 190.5 0.17
determine the influence of each predictor within each model. Multi­ memory
collinearity (VIF and mean VIF) and auto-correlation (Durbin-Watson PDCRS_naming 18.20 (1.78) 18.52 (1.07) 152 0.73
PDCRS_attention 9.30 (1.61) 9.52 (0.68) 146.5 0.89
test) diagnostics were carried out for each of the models. We performed
PDCRS_working memory 5.38 (2.61) 7.89 (1.57) 236 0.004**
this analysis for each of the three APACS composite scores and each of PDCRS_clock drawing 9.62 (0.81) 9.10 (1.27) 124.5 0.52
the sub-scores. PDCRS_copy of a clock 9.37 (0.98) 9.63 (0.53) 162 0.46
All statistical analyses were conducted using R software (Core, PDCRS_delayed verbal 6.84 (1.68) 7.69 (2.02) 177 0.23
2015). memory
PDCRS_alternate fluency 13.03 (4.31) 17.49 (3.21) 236 0.004**
PDCRS_action fluency 17.98 (4.94) 21.74 (3.74) 225 0.01*
5. Results PDCRS_subcortical 73.33 (11.66) 85.50 (8.50) 227 0.003**
PDCRS_cortical 28.18 (2.72) 28.41 (1.22) 151 0.76
5.1. Between-group analyses PDCRS_Total 102.03 (13.39) 114.73 225 0.004**
(8.96)
Semantic memory 1 37.07 (1.70) 38.40 (1.60) 190.5 0.023*
5.1.1. APACS Semantic memory 2 62.33 (1.30) 62.63 (2.03) 143.5 0.21
Table 2A reports the descriptive statistics and the details of the RTME 21.40 (3.88) 22.45 (3.36) 176 0.38
Wilcoxon rank sum tests comparing patients with PD and healthy con­ EAT 23.00 (4.07) 25.50 (5.13) 201.5 0.08
trols for each of the APACS sub-scores and composite scores. Patients Advanced ToM 9.66 (1.23) 10.26 (2.05) 170 0.33
BDI-II 11.06 (9.23) 7.25 (5.85) 128.5 0.31
with PD scored significantly lower than controls in the APACS Total

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M.A. Baraldi et al. Brain and Cognition 150 (2021) 105706

Wilcoxon rank sum tests comparing patients with PD and healthy con­ small number of patients obtained ESs equal to 0 in cognitive tests
trols for each of the cognitive tests. Patients with PD scored significantly (number of patients with ES = 0/total number of patients): Digit span
lower scores than controls in the Corsi Span backward version (visuo- forward: 2/18; Phonemic fluency: 1/18; Corsi forward: 1/18; Corsi back­
spatial working memory -p = 0.011), the time interference effect of the ward: 1/18; Stroop accuracy: 2/18. As for BDI-II, patients’ depression
Stroop test (inhibition -p = 0.05), the Trial Making test (p = 0.045), the ratings were classified as mild (3/18), moderate (2/18), and severe (1/
Semantic Memory 1 task (p = 0.023) and some of the tasks of the PD-CRS 18), according to fixed score ranges (see Appendix for details).
(working memory -p = 0.004; alternate fluency -p = 0.004; action Different results emerged in the control group (number of healthy
fluency -p = 0.01) as well as composite scores (PD-CRS subcortical -p = participants with ES = 0/total number of healthy participants): Corsi
0.003; Total score -p = 0.004). No significant between-group difference forward: 1/21; Stroop time: 1/21. As for BDI-II, controls’ depression
emerged in the depression status (BDI-II). ratings were classified as mild (2/21), and moderate (1/21).

5.2. Participants’ individual performance in APACS


5.4. Correlational analyses

We also evaluated participants’ performance in each pragmatic task


5.4.1. PD group
at the individual level by investigating whether their performance in the
Table 3(A) reports the details of the pairwise Pearson’s correlations
APACS tasks and composite scores was below normative cut-off. A
between PD patients’ scores in APACS and their scores in the cognitive
considerable number of patients showed a performance below cut off in
tests as well as their demographic variables. Results revealed that, in the
the production tasks and composite score (number of patients below cut-
PD group, the APACS Total score was negatively correlated with age (r
off/total number of patients: Interview task: 12/18; Description task 13/
= − 0.49; p = 0.038) and positively correlated with PD-CRS total score, a
18; Pragmatic Production 16/18). Furthermore, several patients also
measure of general cognitive skills (r = 0.53; p = 0.038). Pragmatic
showed an impaired performance in two of the comprehension tasks and
Comprehension negatively correlated with age (r = − 0.49; p = 0.036)
in the comprehension composite score (Narratives task: 10/18; Figurative
and positively correlated with education (r = 0.56; p = 0.013) and with
Language 2 task: 9/18; Pragmatic Comprehension: 6/18). Similarly, a
the forward version of the Corsi test, which evaluates short-term visuo-
consistent number of PD patients obtained an impaired performance in
spatial memory (r = 0.48; p = 0.049). Pragmatic Production was
the APACS Total score (11/18). Different results emerged in the control
negatively correlated with education (r = − 0.49; p = 0.036), the
group (number of healthy participants below cut-off/total number of
severity of motor symptoms – the MDS UPDRS III score (r = − 0.50; p =
healthy participants): Interview task: 2/21; Description task 13/21; Prag­
0.034), shifting, measured with the TMT score (r = − 0.63; p = 0.0047),
matic Production 11/21; Narratives task: 6/21; Humor task: 2/21; Figu­
and positively correlated with the PD-CRS total score (r = 0.77; p =
rative Language 2 task: 2/21; Pragmatic Comprehension: 2/21; APACS
0.0007) and the EAT score, a measure of affective ToM (r = 0.60; p =
Total score: 3/21.
0.016).
With respect to each APACS task, Interview was negatively corre­
5.3. Participants’ individual cognitive performance lated with education (r = -0.47; p = 0.046), the TMT score (r = − 0.61; p
= 0.006) and the MDS UPDRS III score (r = − 0.48; p = 0.04), and it is
The neuropsychological performance was also explored at the indi­ positively correlated with the PD-CRS Total score (r = 0.57; p = 0.025).
vidual level by investigating whether participants obtained equivalent Description negatively correlated with the TMT score (r = − 0.48; p =
scores (ES) equal to 0 (indicating impaired performance) in the selected 0.041) and with the error interference effect of the Stroop task (r =
neuropsychological tests with available correction grids. A relatively − 0.57; p = 0.016), and positively correlated with the PD-CRS Total

Table 3A
Person Correlation coefficients in patients with PD (A) between APACS tasks and the other clinical, demographic and cognitive variables. Asterisks indicate significant
correlations: ** p < 0.01, * p < 0.05.
APACS Interview Description Narratives Figurative Humor Figurative Pragmatic Pragmatic APACS
Language 1 Language 2 Production Comprehension Total

Age 0.08 − 0.3 − 0.49* − 0.2 − 0.26 − 0.45 − 0.15 − 0.49* − 0.49*
Education − 0.47* − 0.38 0.42 0.13 0.47* 0.5* − 0.49* 0.56* 0.2
Sex 0.2 0.21 0.024 0.23 − 0.13 0.18 0.23 0.05 0.16
UPDRS III − 0.48* − 0.38 0.013 0.19 0.09 0.06 − 0.50* 0.1 − 0.18
Years from Onset − 0.17 0.2 0.064 0 − 0.041 0.28 0.04 0.1 0.1
Digit Span_forward 0.46 0.3 0.15 0.25 − 0.1 0.25 0.44 0.13 0.34
Digit − 0.1 − 0.1 0.05 0.21 0.18 − 0.054 − 0.12 0.12 0.035
Span_backward
Phonemic fluency 0.35 0.15 0.38 0.17 − 0.07 0.19 0.28 0.2 0.32
Semantic fluency 0.1 0.53* 0.29 0.11 − 0.027 0.21 0.41 0.19 0.37
Corsi_forward 0.13 0.05 0.44 − 0.24 0.45 0.44 0.1 0.48* 0.45
Corsi backward − 0.28 − 0.002 0.17 − 0.3 0.23 − 0.02 − 0.14 0.11 0.02
BDI-II − 0.34 − 0.34 − 0.019 − 0.09 0.04 − 0.26 − 0.4 − 0.09 − 0.28
Stroop accuracy − 0.1 − 0.57* − 0.12 0.005 0.31 − 0.03 − 0.42 0.08 − 0.15
Stroop time − 0.28 − 0.17 − 0.26 0.19 − 0.31 − 0.04 − 0.26 − 0.22 − 0.32
TMT − 0.61** − 0.48* 0.03 − 0.04 0.024 0.013 − 0.63** 0.02 − 0.32
PD-CRS working 0.34 0.18 0.41 0.11 0.11 0.4 0.29 0.36 0.45
memory
PD-CRS total 0.57* 0.7** 0.29 0.17 − 0.046 0.11 0.77** 0.15 0.53*
Semantic memory 0.06 − 0.12 − 0.13 0.04 − 0.42 0.21 − 0.03 − 0.15 − 0.15
1
Semantic memory − 0.008 0.31 0.2 − 0.02 − 0.26 0.09 0.16 − 0.015 0.065
2
RTME 0.29 0.14 0.27 − 0.13 − 0.013 0.1 0.24 0.11 0.22
EAT 0.41 0.58* − 0.009 − 0.08 − 0.26 0.004 0.6* − 0.12 0.21
Advanced ToM 0.1 0.14 0.078 0.02 − 0.036 0.05 0.15 0.035 0.11

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M.A. Baraldi et al. Brain and Cognition 150 (2021) 105706

score (r = 0.71; p = 0.002), with the EAT score (r = 0.58; p = 0.021) and f). These analyses revealed that the global score of the PD-CRS (p =
with semantic fluency (r = 0.53; p = 0.026). Narratives was negatively 0.008) and education (p = 0.012) significantly predicted participants’
correlated with age (r = − 0.49; p = 0.038). Participants’ scores in the APACS Total score. The Production Total score was significantly pre­
Humor task (r = 0.47; p = 0.045) and in the Figurative Language 2 task dicted by the global score of the PD-CRS (p = 0.0036). Education (p =
(r = 0.5; p = 0.03) positively correlated with education. No significant 0.007) was the only significant predictor of the Comprehension Total
correlations were found between participants’ scores in the Figurative score. The time interference effect of the Stroop test (p = 0.02) predicted
Language 1 task and any of the clinical, demographic and cognitive patients’ performance in the Interview task, while participants’ scores in
measures. the Description task were significantly predicted by the Stroop error
interference effect (p = 0.009), and the total score of the PD-CRS (p =
5.4.2. Control group 0.001). Finally, the Stroop time interference effect (p = 0.0025), the
Table 3(B) reports the details of the pairwise Pearson’s correlations global score of the PD-CRS (p = 0.032), education (p = 0.00017) and sex
between healthy controls’ scores in APACS and their scores in the (p = 0.012) were significant predictors of the Figurative Language 2
cognitive tests as well as their demographic variables. The APACS Total task.
score was negatively correlated with both the time (r = − 0.45; p =
0.036) and the error (r = − 0.82; p < 0.001) interference effects of the 5.5.2. Control group
Stroop test. These two measures of the Stroop test also negatively Table 5(a-h) reports the statistical details of the multiple regression
correlated with Pragmatic Comprehension (time interference effect r = analyses between healthy controls’ scores in APACS and their scores in
− 0.43; p = 0.05; error interference effect r = − 0.78; p < 0.001). Prag­ the cognitive measures as resulting from the backward stepwise method.
matic Production was negatively correlated only with the error inter­ The Stroop error interference effect was the main significant predictor of
ference effect of the Stroop Test (r = − 0.66; p < 0.001). Interview almost all of the APACS composite scores as well as sub-scores: APACS
negatively correlated with the TMT (r = − 0.54; p = 0.011) and the EAT Total (p < 0.0001); Pragmatic Production (p = 0.002); Pragmatic
score (r = − 0.5; p = 0.023). Description was negatively correlated with Comprehension (p < 0.0001); Description (p = 0.0002); Narratives (p <
the error interference effect of the Stroop test (r = − 0.075; p < 0.001). 0.0001); Figurative Language 1 (p = 0.0089); Humor (p = 0.0047);
Participants’ scores in the Narratives task negatively correlated with Figurative Language 2 (p = 0.024).
both the time (r = − 0.42; p = 0.05) and the error (r = − 0.78; p < 0.001)
interference effects of the Stroop test, and positively correlated with 6. Discussion
education (r = 0.44; p = 0.044). Both Figurative Language 1 (r = − 0.58;
p = 0.005) and Humor (r = − 0.61; p = 0.003) were negative correlated 6.1. Impairment of pragmatic abilities in early PD
with the error interference effect of the Stroop test. No significant cor­
relations were found between participants’ scores in the Figurative This study revealed several interesting findings. First, patients with
Language 2 task and any of the clinical, demographic and cognitive PD exhibited significantly lower scores of APACS Total as compared to
measures. healthy controls. This result was also investigated at the individual level:
the APACS Total score was below cut-off for 61% of the patients. Spe­
cifically, our results showed lower scores in Pragmatic Production for
5.5. Analyses of predictors
patients with early PD as compared to healthy elderly. Interestingly, this
general production score was below cut-off for 88.8% of the patients.
5.5.1. PD group
Finally, the PD group scored lower than controls in Pragmatic
The statistical details of the multiple regression analyses between PD
Comprehension too, and 33.3% of the patients scored below cut-off.
patients’ scores in APACS and their scores in the cognitive measures as
Overall, these results suggest that patients with early PD show worse
resulting from the backward stepwise method are reported in Table 4(a-

Table 3B
Person Correlation coefficients in healthy controls between APACS tasks and the other clinical, demographic and cognitive variables. Asterisks indicate significant
correlations: ** p < 0.01, * p < 0.05.
APACS Interview Description Narratives Figurative Humor Figurative Pragmatic Pragmatic APACS
Language 1 Language 2 Production Comprehension Total

Age − 0.05 − 0.05 − 0.06 0.2 0.005 0.28 − 0.06 0.11 0.05
Education − 0.33 0.15 0.44* 0.12 0.17 0.42 0.04 0.39 0.28
Sex − 0.02 − 0.09 − 0.05 0.12 − 0.21 0.1 − 0.09 − 0.15 − 0.14
Digit Span_forward − 0.42 − 0.28 − 0.24 − 0.13 0.11 − 0.03 − 0.37 − 0.05 − 0.2
Digit − 0.23 − 0.09 − 0.1 − 0.002 0.3 0.32 − 0.15 0.23 0.09
Span_backward
Phonemic fluency 0.23 0.005 − 0.19 0.12 0.21 0.26 0.07 0.15 0.13
Semantic fluency 0.26 0.28 0.17 0.19 0.31 0.19 0.32 0.32 0.36
Corsi_forward 0.09 0.02 0.05 0.12 0.34 0.002 0.04 0.21 0.16
Corsi_backward 0.07 0.06 − 0.3 − 0.02 0.14 − 0.13 0.07 − 0.07 − 0.01
BDI-II 0.06 0.17 − 0.096 0.29 0.11 0.095 0.17 0.11 0.15
Stroop accuracy 0.01 − 0.75** − 0.78** − 0.58** − 0.61** − 0.32 − 0.66** − 0.78** − 0.82**
Stroop time − 0.23 − 0.33 − 0.42* − 0.27 − 0.25 − 0.36 − 0.36 − 0.43* − 0.45*
TMT − 0.54* − 0.18 − 0.03 0.17 − 0.11 0.17 − 0.31 0.02 − 0.12
PD-CRS working − 0.27 0.11 0.28 0.08 0.08 0.21 0.02 0.19 0.14
memory
PD-CRS total 0.33 0.26 0.13 0.2 0.15 − 0.01 0.32 0.15 0.24
Semantic memory − 0.31 0.21 0.26 0.09 − 0.01 0.04 0.1 0.1 0.12
1
Semantic memory − 0.13 0.26 0.29 − 0.29 − 0.12 − 0.17 0.2 − 0.065 0.043
2
RTME 0.22 0.1 − 0.03 0.16 − 0.08 − 0.21 0.15 − 0.09 0.006
EAT − 0.5* 0.09 0.42 − 0.11 0.01 − 0.08 − 0.05 0.1 0.04
Advanced ToM 0.17 0 0.28 0.03 0.18 0.03 0.05 0.2 0.15

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Table 4 general pragmatic abilities (the ability to perform a cluster of different


(a-f). Predictors of pragmatic abilities in the PD group. Asterisks indicate sig­ pragmatic tasks in language production and comprehension, estimated
nificant predictors: ** p < 0.01, * p < 0.05. with a total score – the APACS Total score) as compared to healthy
a. Predictors of APACS Total elderly; this is also particularly evident for Pragmatic Comprehension
Adjusted R2 p Mean VIF Test for autocorrelation
and, most of all, for Pragmatic Production. In fact, patients’ production
skills are more compromised, as compared to comprehension abilities.
D-W p
These results are consistent with Montemurro and colleagues (2019),
0.61 0.013 2.30 2.76 0.068 who also found compromised performance in the three APACS com­
posite scores in the sample of patients with PD, compared to healthy
Predictor Estimate βi p VIF
controls. Most important, our results suggest that pragmatic skills are
(Intercept) 0.63 0.0097** already impaired at the early stage of the disease. In sum, a general
Stroop_time − 0.002 − 0.43 0.11 2.32
impairment of pragmatic abilities in subjects diagnosed with PD seems
PD-CRS Total 0.0037 0.89 0.008** 2.63
age − 0.002 − 0.25 0.19 1.21 to emerge both in comprehension and production. Our findings provide
education 0.013 0.85 0.012* 2.77 an important contribution to our understanding of pragmatic abilities in
sex − 0.073 − 0.53 0.074 2.56 PD, as they show a deficit of pragmatic skills in a sample of patients with
b. Predictors of APACS Pragmatic Production early-course PD. Early detection of general pragmatic impairment for
Adjusted R2 p mean VIF Test for autocorrelation
both production and comprehension is crucial in order to monitor its
progression over time, as pragmatic deficit plays a crucial role in pa­
D-W p
tients’ daily living and in the way people can successfully communicate
0.70 0.002 1.50 1.91 0.8 in social interactions.
Predictor Estimate βi p VIF Second, with respect to the single APACS tasks, we found that pa­
(Intercept) 0.65 <0.001**
Stroop_accuracy − 0.006 − 0.26 0.11 1.14
tients with PD achieved lower scores in the Interview and the Figurative
Stroop_time − 0.0016 − 0.26 0.17 1.56 Language 2 tasks, as compared to healthy controls. At the individual
PD-CRS Total 0.003 0.73 0.0036** 1.81 level, 66.6% of patients performed below cut-off in the Interview task,
sex − 0.048 − 0.33 0.085 1.41 showing difficulties mainly in discourse organization, engagement in
c. Predictors of APACS Pragmatic Comprehension conversations, as well as in non-verbal dimensions. Furthermore, half of
Adjusted R2 p Mean VIF Test for autocorrelation the PD sample was actually impaired in the Figurative Language 2 task,
showing difficulties in non-literal language understanding, such as
D-W p
proverbs, idioms and novel metaphors. Similarly, Montemurro et al.
0.54 0.0086 1.26 2.63 0.126 (2019) observed a significant lower performance of patients with PD in
Predictor Estimate p VIF
βi
the Interview task; on the contrary, the authors showed that the group of
(Intercept) 0.76 0.034*
PD-CRS Total 0.0024 0.35 0.11 1.36 PD patients achieved significant lower scores also in the Description,
age − 0.0053 − 0.36 0.087 1.13 Narratives and Humor tasks as compared to healthy controls, which did
education 0.017 1.30 0.007** 1.30 not emerge in our study. The discrepancies between these findings might
d. Predictors of APACS Interview task be related to the differences in the sample of PD patients: we recruited
patients with early PD (H&Y < 2), whereas Montemurro and colleagues
Adjusted R2 p mean VIF Test for autocorrelation
focused on a sample of patients whose symptom severity was highly
D-W p
heterogenous (H&Y 1–4), finding a more widespread pragmatic deficit.
0.42 0.014 1.12 1.38 0.22 Interestingly, our findings did not show any significant between-
Predictor Estimate βi p VIF group difference in the Figurative Language 1 task, while this was the
(Intercept) 45.98
case for the Figurative Language 2 task. Despite both tasks assess the
<0.001**
Stroop_time − 0.15 − 0.56 0.02* 1.12
MDS UPDRS III − 0.1 − 0.28 0.21 1.12 ability to understand non-literal uses of language (idioms, novel meta­
phors and proverbs), they are carried out with different modalities. The
e. Predictors of APACS Description task
first one consists of multiple-choice questions and only requires partic­
Adjusted R2 p Mean VIF Test for autocorrelation ipants to select the correct interpretation out of three possible options.
D-W p Importantly, the response choices remain always available to the par­
0.71 0.0006 1.35 2.15 0.82 ticipants while performing the task. In other words, the characteristics of
Predictor Estimate βi p VIF this task seem simple enough to likely reduce cognitive effort. On the
(Intercept) 23.81 <0.001** contrary, the second task is more complex, as it assesses comprehension
Stroop_accuracy − 0.69 − 0.46 0.009** 1.09
by asking the participants to orally paraphrase non-literal expressions.
PD-CRS Total 0.22 0.76 0.001** 1.51
sex − 3.09 − 0.32 0.08 1.45
While Figurative Language 1 simply tests participants’ ability to select
the contextually appropriate interpretation of a figurative expression,
f. Predictors of APACS Figurative Language 2 task
Figurative Language 2 taps on a more genuine understanding of the
Adjusted R2 p Mean VIF Test for autocorrelation expression, as participants are required to autonomously derive the
D-W p appropriate non-literal meaning – i.e., no constraint that might support
0.78 0.0012 2.30 1.70 0.59
interpretation is provided. Therefore, contrary to Figurative Language 1,
Predictor Estimate βi p VIF Figurative Language 2 elicits an interpretive process that is more
(Intercept) 12.8 0.23 cognitively demanding, but also more ecological.
Stroop_time − 0.32 − 0.78 0.0025** 2.32
PD-CRS Total 0.14 0.51 0.032* 2.63
age − 0.12 − 0.20 0.17 1.21
6.2. Cognitive functioning in early-course Parkinson’s disease
education 1.39 1.27 0.00017** 2.77
sex − 5.90 − 0.62 0.012* 2.56 We assessed between-group differences in a cluster of cognitive
functions. Patients with PD obtained a worse performance in visuo-
spatial working memory, inhibition, set-shifting and cognitive flexi­
bility, verbal working memory, alternate and action fluency, and se­
mantic memory. The total score of the PD-CRS suggested that PD

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M.A. Baraldi et al. Brain and Cognition 150 (2021) 105706

Table 5
(a-h). Predictors of pragmatic abilities in the control group of healthy elders. Asterisks indicate significant predictors: ** p < 0.01, * p < 0.05.
a. Predictors of APACS Total
Adjusted R2 p Mean VIF Test for autocorrelation

D-W p

0.69 <0.0001 1 1.96 0.83

Predictor Estimate βi p VIF

(Intercept) 0.78 <0.0001**


Stroop_accuracy − 0.08 − 0.81 <0.0001** 1
PD-CRS Total 0.001 0.18 0.18 1

b. Predictors of APACS Pragmatic Production


Adjusted R2 p Test for autocorrelation

D-W p

0.46 0.0027 1.89 0.74

Predictor Estimate βi p VIF

(Intercept) 0.75 <0.0001**


Stroop_accuracy − 0.05 − 0.64 0.002** 1
PD-CRS Total 0.0015 0.27 0.13 1

c. Predictors of APACS Pragmatic Comprehension

Adjusted R2 p Test for autocorrelation

D-W p

0.62 <0.0001 2.35 0.47

Predictor Estimate βi p

(Intercept) 0.9 <0.0001**


Stroop_accuracy − 0.1 − 0.8 <0.0001**

d. Predictors of APACS Description task

Adjusted R2 p Test for autocorrelation

D-W p

0.54 0.0002 1.8 0.63

Predictor Estimate βi p

(Intercept) 43.52 <0.0001**


Stroop_accuracy − 5.48 − 0.75 0.0002**

e. Predictors of APACS Narratives task


Adjusted R2 p Test for autocorrelation

D-W p

0.61 <0.0001 2.16 0.75

Predictor Estimate βi p

(Intercept) 51.01 <0.0001**


Stroop_accuracy − 7.54 − 0.79 <0.0001**

f. Predictors of APACS Figurative Language 1 task

Adjusted R2 p Test for autocorrelation

D-W p

0.29 0.0089 1.32 0.096

Predictor Estimate βi p

(Intercept) 14.59 <0.0001**


Stroop_accuracy − 0.82 − 0.58 0.0089**

g. Predictors of APACS Humor task


Adjusted R2 p Test for autocorrelation

D-W p

0.34 0.0047 2.19 0.73

Predictor Estimate βi p

(Intercept) 6.51 <0.0001**


Stroop_accuracy − 1.2 − 0.61 0.0047**

h. Predictors of APACS Figurative Language 2 task

(continued on next page)

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M.A. Baraldi et al. Brain and Cognition 150 (2021) 105706

Table 5 (continued )
Adjusted R2 p Test for autocorrelation

D-W p

0.22 0.024 2.6 0.17

Predictor Estimate βi p

(Intercept) 24.63 <0.0001**


Stroop_accuracy − 2 − 0.51 0.024*

patients show worse general cognitive skills (i.e., lower overall cognitive impairment and executive dysfunction might act as underlying mecha­
level) as compared to healthy controls, consistently with previous nisms of PD patients’ compromised pragmatic production (Colman &
studies (McKinlay et al., 2009; Papagno & Trojano, 2018). We did not Bastiaanse, 2011; Holtgraves et al., 2013). Importantly, different results
find any significant difference at the group level in the BDI-II score, emerged in the group of healthy participants. In this population,
which means that the depression status in the two groups was compa­ inhibitory control (i.e., the error interference effect of the Stroop test)
rable; in light of the possible association between depression and was the only predictor of both general pragmatic abilities and Pragmatic
cognitive abilities (Crocco et al., 2010), this result might allow us to Production. More specifically, participants who were more accurate in
state that patients’ lower cognitive performance was not related to the this test scored higher in most of the APACS tasks. Taken together, these
presence of higher levels of depression in the PD group. Interestingly, we findings suggest that inhibitory control plays an important role in per­
did not find any significant difference at the group level in any of the forming different pragmatic tasks in both groups; however, intact gen­
administered ToM tasks, and this might be due to the early stage of the eral cognitive skills and higher education might act as compensatory
disease. In fact, a previous study by Péron and colleagues (2009) showed mechanisms, supporting PD patients’ general pragmatic competence
that early PD patients’ ToM performance did not significantly differ and production abilities. Overall, despite the importance of unimpaired
from that of healthy participants. Moreover, the authors did not find any cognitive skills and high education levels, we believe that other factors
significant difference between medicated and unmedicated patients in might support PD patients’ pragmatic performance, as reported by
the early PD group. Conversely, a specific ToM impairment at the previous literature (Colman & Bastiaanse, 2011), and this represents an
cognitive level (Péron et al., 2009) and at the affective level (Raffo De interesting starting point for future investigation targeting more
Ferrari et al., 2015) was found in advanced PD patients. In sum, in line advanced stages of the disease.
with previous studies, our findings suggest that the mind-reading ability
is still intact in both its affective and cognitive components in patients 6.3.2. Predictors of pragmatic comprehension: Understanding non-literal
with early-course PD. meaning
An interesting scenario emerged on the predictors of our partici­
pants’ pragmatic comprehension. The control group scored significantly
6.3. Predictors of pragmatic skills higher than the PD group in general pragmatic comprehension as well as
in the Figurative Language 2 task, and the only significant predictor of
We conducted a set of analyses of predictors to investigate the in­ healthy controls’ performance in these two measures was accuracy in
fluence of some cognitive functions and demographic variables on early the Stroop task. Overall, this pattern suggests that healthy participants
PDs’ pragmatic abilities. First, a broad pattern emerged: the predictors exhibit uncompromised pragmatic comprehension abilities. As for the
that significantly influenced general pragmatic abilities, pragmatic role of accuracy in the Stroop task, this is not particularly informative
production and pragmatic comprehension were not the same in the because in the Stroop task the most genuine measure for inhibitory
group of PD patients and in the control group. We now discuss these in control is the time interference effect (i.e., the time needed to inhibit a
turn. highly salient information), rather than accuracy. On the contrary,
interestingly, a substantially different pattern of results emerged in the
6.3.1. Predictors of general pragmatic skills and pragmatic production group of PD patients. PD patients’ general pragmatic comprehension
We conducted a set of analyses of predictors to verify the influence of was significantly predicted by education only. Even more interesting, a
some cognitive functions and demographic variables on both early PDs’ cluster of cognitive functions and demographic variables significantly
and healthy controls’ pragmatic abilities. Interestingly, different pat­ predicted patients’ performance in the Figurative Language 2 task, that
terns of results emerged in the two groups. Within the PD group, general assesses figurative expressions such as novel metaphors and idioms
pragmatic abilities were significantly predicted by general cognitive understanding. The cluster included inhibitory control (i.e., time inter­
skills and education. More specifically, our data show that patients with ference effect), general cognitive skills, and education. Similarly, exec­
better general cognitive skills scored higher in the APACS Total. Addi­ utive impairment has been previously related to poor performance in
tionally, with respect to demographic variables, patients with higher novel metaphor comprehension in other clinical populations, such as
education exhibited a better general pragmatic performance. Our results Alzheimer’s Disease (AD) (Amanzio et al., 2008). As for the role of ed­
are consistent with the existing literature, as cognitive skills have been ucation, PD participants with higher education showed less impaired
previously linked to pragmatic abilities (Bosco, Parola, Sacco, Zettin, & comprehension abilities. Education is notably known as a socio-
Angeleri, 2017; Colman & Bastiaanse, 2011; Holtgraves et al., 2013); demographic factor that positively impacts individuals’ cognitive
furthermore, pragmatic competence has been found to be less efficient in reserve, thus acting as a protective factor (Da Silva et al., 2015). In
people and lower education (Zanini, Bryan, De Luca, & Bava, 2005). As addition, old adults with higher education were found to exhibit better
for PD patients’ general production abilities, the global score of the PD- metaphor understanding (Champagne-Lavau, Monetta, & Moreau,
CRS was the only significant predictor of the Pragmatic Production 2012) and socio-demographic factors were recently posited to influence
composite score, suggesting that intact general cognitive skills individuals’ metaphor comprehension (Gibbs & Colston, 2012). In light
contribute to a better general production performance as well. of this, therefore, it might be the case that education acts as a protective
Furthermore, as for the two production tasks, inhibition significantly factor in PD pragmatic comprehension abilities too, including the ability
predicted both Interview and Description; more specifically, patients to understand non-literal meaning.
with better inhibitory control scored higher in both tasks. These findings Interestingly, inhibitory control accounted for 78% of the variance in
are consistent with earlier research suggesting that cognitive

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M.A. Baraldi et al. Brain and Cognition 150 (2021) 105706

PD patients’ comprehension of figurative expressions such as novel As for idioms, the role of inhibitory mechanisms has been called for
metaphors and idioms. More specifically, participants with better scores also with respect to this figurative use of language (Cacciari, Corrardini,
in the time interference effect of the Stroop test, were also more accurate & Ferlazzo, 2018; Galinsky & Glucksberg, 2000). Some studies on id­
in providing a good interpretation of the non-literal expressions pre­ ioms processing suggest that a momentary activation of at least part of
sented in the Figurative Language 2 task. This finding suggests that the literal meaning of the words that compose the idiomatic expression
inhibitory control predicts figurative language comprehension in early- occur during idioms interpretation (Cacciari, Padovani, & Corradini,
course PD. To the best of our knowledge, this is first evidence of the role 2007; Holsinger & Kaiser, 2013). Futhermore, according to Cacciari
of inhibitory control in early-course PD understanding of figurative et al. (2018), suppression mechanisms of the literal meaning of the
meanings and this prevents us from discussing the finding with previous words that compose idiomatic expressions may take place and the
experimental data on PD. However, the role of inhibitory control has activation of the literal meaning may depend on some psycholinguistic
been previously addressed in experiments on young healthy adults’ factors, such as the predictability of the expression. During the pro­
interpretation of novel metaphors and idioms. As for metaphor, inhibi­ cessing of predictable idioms, such as My brother is always broke, the
tory control was found to predict adolescents’ metaphor interpretation literal meaning of the constituent words that appear first in the
(Carriedo et al., 2016). Furthermore, inhibitory control might be expression might suffice to pre-activate the constituent words that are
essential to suppress those properties of the metaphor literal meaning more likely to appear next - in virtue of the predictability of the whole
that are not essential to derive the metaphorical interpretation. In fact, idiomatic expression. Once the activated literal interpretation becomes
some studies have shown that the literal meaning of the expression is irrelevant for the idiomatic meaning, the literal meaning is actively
activated during early processing of novel metaphors, and that it is suppressed. Therefore, based on this, our results suggest that idioms
suppressed later on (Rubio Fernández, 2007; Weiland, Bambini, & comprehension is impaired already in early-course PD. Yet, more effi­
Schumacher, 2014). Additionally, it has been shown that the irrelevant cient inhibitory skills still might facilitate idioms comprehension too: PD
properties of the literal meaning of the metaphor vehicle (e.g., ‘Some participants with more preserved inhibitory control might have more
hairstyles are bushes’) are suppressed during metaphor interpretation easily suppressed the activated literal meaning of the expressions under
and this has been associated with the role of inhibitory control scrutiny, which might have favoured their comprehension of idioms.
(Glucksberg, Newsome, & Goldvarg, 2001). The main idea behind these Our findings concerning the involvement of inhibitory processes in
studies is consistent with a direct access view of metaphor interpreta­ non-literal language comprehension are consistent with the hypothesis
tion2 (Gibbs, 1994; Wilson & Carston, 2007). According to this broad linking PD patients’ common frontal lobe dysfunction to pragmatic
view, metaphorical meaning is accessed directly in online processing difficulties (McNamara & Durso, 2003; Monetta & Pell, 2007). Executive
and the interpretation of literal meaning does not play any special role deficits are typically associated with dysfunctions of the dorsolateral
apart from providing a hint for the derivation of the metaphor. To put it prefrontal cortex (DLPFC), and the anterior cingulate cortex (ACC)
simple, the theoretical accounts that support a direct access view for (MacDonald, Cohen, Stenger, & Carter, 2000), which seem to be
metaphor interpretation differ in many respects – for example, contrary impaired in PD (Palermo et al., 2017). While the DLPFC is involved in
to Gibbs (1994), Wilson & Carston (2007) see metaphor comprehension attentional processes, planning, sequencing, and working memory , the
as the outcome of a process of pragmatic adjustment based on ad hoc ACC is engaged in evaluative processes, such as detecting the presence of
concepts construction.3 Importantly, however, the direct access views response conflict and, more in general, in inhibitory control (MacDon­
agree on the fact that literal meaning would be involved in the inter­ ald, Cohen, Stenger, & Carter, 2000; Weintraub et al., 2005). This
pretive process only to the extent that the relevant literal properties of dissociation is confirmed by previous neuroimaging studies analyzing
the metaphor vehicle (e.g., bushes are MESSY) are pragmatically participants’ performance in the Stroop task. In the incongruent condi­
adjusted such that they can be meaningfully exploited to derive the tion, greater activity within the ACC has been detected (Pardo, Pardo,
metaphorical meaning. On the contrary, the irrelevant properties of the Janer, & Raichle, 1990), reflecting a greater effort in terms of inhibitory
vehicle literal meaning (e.g., bushes are GREEN) would not be used in skills. Conversely, the DLPFC activity might reflect the sustained
the interpretive process and, after an initial activation, they would be attention required to complete the task, which is also particularly
readily suppressed. In this wider scenario, therefore, it is reasonable that evident in the simple color naming condition. In sum, the impairment of
patients with better inhibitory skills exhibited a better interpretation of the DLPFC and ACC in patients with PD might be responsible for deficits
novel metaphors because they might have been more efficient in sup­ of inhibitory control, and this is consistent with our findings showing
pressing the irrelevant literal properties, which in turn might have that patients with lower inhibitory skills (in terms of longer response
enhanced metaphor comprehension. In sum, our findings show that times in the Stroop task) exhibit greater difficulties in suppressing the
early PD patients’ ability to comprehend figurative language is irrelevant literal properties during metaphor and idiom comprehension.
impaired, as indicated by differences at both the individual and group
levels. Yet, inhibitory control might act as a compensatory mechanism 7. Conclusions
and might support a better comprehension of metaphor, likely because
more preserved inhibitory skills enhance the suppression of the irrele­ This study has several important clinical implications. From a clin­
vant literal properties of a novel metaphor. ical point of view, the early detection of pragmatic deficits is crucial
because this disorder directly impacts the way people communicate in
social contexts. Deficits in pragmatic production, that include discourse
organization and engagement in communication, as well as pragmatic
2
This branch of the theoretical debate on metaphor comprehension devel­ comprehension might be responsible for a reduction in social interaction
oped in contrast to the indirect access view (Grice, 1975; Searle, 1979), according and a decrease in socialization due to the arise of communication dif­
to which metaphor interpretation is derived inferentially as an implicature only ficulties. An early identification of these deficits seems essential to
after the false literal meaning is passed through and rejected as false. monitor their progression over time. To this purpose, it would be worth
3
In metaphors like My lawyer is a shark, the literal meaning is quickly
monitoring patients’ quality of life too in future studies. In fact, not only
reworked online into a metaphorical meaning through the ad-hoc concept
both pragmatic deficits and quality of life strongly impact social in­
construction. In other words, the lexically encoded concept SHARK is quickly
adjusted into the ad-hoc concept SHARK*, whose denotation also includes teractions, but also pragmatic impairment may play a role in any change
specific types of human beings (ruthless, merciless etc.). In routinized examples of patients’ quality of life. Therefore, both aspects should be monitored
like ‘shark’, ‘devil’, ‘saint’, ‘block of ice’ etc., ad-hoc concepts are constructed complementarily. Moreover, the results of this study represent an
online, and the associated metaphorical meaning is therefore immediately interesting starting point for future investigations. To start with, prag­
activated. matic abilities should be explored in advanced stages of PD, that are

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M.A. Baraldi et al. Brain and Cognition 150 (2021) 105706

characterized by more invalidating motor disabilities and progressive repeat these in the same order as the digits were presented to them. The
cognitive changes. It would be worth focusing more on nonverbal length of the lists gradually increases from three to nine digits. After
pragmatic skills in patients with advanced PD, in light of the potential each list, if participants correctly repeat the set of digits, another list one
link with motor symptoms. In addition, it would be worth investigating digit longer is presented; if they fail, a second list of the same length is
further PD patients’ understanding of figurative language, especially presented. If subjects succeed the second list, a list one digit longer is
metaphor, and the role of inhibitory control. presented. If they fail on the second list, the test is ended. The span is
Finally, this study has at least two limitations worth acknowledging. established as the length of the longest list correctly recalled. The final
First, the relatively small sample size implies the need to replicate our score is then corrected for age and education (Monaco et al., 2013).
findings with larger samples. Second, contrary to previous studies Digit Span backward (Monaco et al., 2013). The procedure is the same
(Bambini, Arcara, Bechi, et al., 2016; Bambini, Arcara, Martinelli, et al., as for the forward version, except that participants are now asked to
2016; Montemurro et al., 2019), we did not assess receptive language repeat the digits sequences in the reverse order and the longest list
abilities as we wanted to focus on a wider range of neuropsychological consists of eight items. The scoring is the same as for the forward version
functions. However, the evaluation of language comprehension is (Monaco et al., 2013).
crucial to exclude any possible link between impaired basic receptive Corsi Span forward (Monaco et al., 2013; Spinnler & Tognoni, 1987).
skills and pragmatic difficulties. For this reason, only participants The experimental apparatus consists of a wooden board with nine cubic
reaching cut-off scores in tests assessing basic language comprehension blocks. A serial number (from 1 to 9) is located on each block and this is
should be enrolled in future studies. visible only to the examiner. Following a given numerical sequence, the
examiner touches sequences of blocks that may range from 3 to 9 blocks.
Funding sources For each sequence, participants are asked to touch the blocks in the same
order as the examiner. The first sequence includes 3 blocks. If partici­
This research did not receive any specific grant from funding pants fail, a second sequence of the same length is presented. If they
agencies in the public, commercial, or not-for-profit sectors. succeed, a sequence one block longer is given. The test ends when
participants fail on two consecutive sequences of the same length. The
CRediT authorship contribution statement span is computed as the length of the longest sequence correctly
reproduced. The final score is then corrected for age and education
Maria Alice Baraldi: Conceptualization, Methodology, Investiga­ (Monaco et al., 2013).
tion, Formal analysis, Writing - original draft. Laura Avanzino: Meth­ Corsi Span backward (Monaco et al., 2013). The procedure and
odology, Supervision. Elisa Pelosin: Methodology, Supervision. Filippo scoring are the same as for the forward version, except that now par­
Domaneschi: Methodology, Supervision, Writing - review & editing. ticipants are asked to reproduce the sequence of blocks in the reverse
Simona Di Paola: Formal analysis, Writing - review & editing. Gio­ order and that the longest list includes eight items (Monaco et al., 2013).
vanna Lagravinese: Methodology, Investigation, Supervision. Verbal fluency test (Novelli et al., 1986). The semantic categories
were animals, fruits and car brands. The phonemic categories included
Declaration of Competing Interest words beginning with the letters F, P and L. Two scores are obtained, one
for semantic fluency and the other for phonemic fluency. In both cases,
The authors declare that they have no known competing financial the score is obtained by counting the number of correct responses (1
interests or personal relationships that could have appeared to influence score for each correct response) and correcting this for age and
the work reported in this paper. education.
Trail Making Test (TMT) (Mondini, Mapelli, Vestri, & Bisiacchi,
Acknowledgments 2003). It is made up of two parts, A and B. In Part A, participants are
required to connect 25 numbered circles with direct line in ascending
We would like to thank all the patients and participants for their kind order (i.e., 1-2-3-4…); in Part B, participants are asked to connect
cooperation. We thank two anonymous reviewers, as well as all the numbered and lettered circles in alternated numerical and alphabetical
participants in the 3rd Experimental Pragmatics in Italy Conference order (i.e., 1-A-2-B-3-C…). A composite score is obtained by subtracting
(XPRAG.it 2019), University of Cagliari, September 19-20 2019 for the the time for A to the time for B (i.e., B-A). The final score is then cor­
constructive comments. In particular, we thank Valentina Bambini and rected for age and education (Siciliano, Chiorri, & Battini, 2019).
Giorgio Arcara for helpful discussion and comments at various stages of Stroop test (short version) (Caffarra et al., 2002; Venneri et al., 1992).
this work. Participants are required to read aloud three lists of items as fast as
possible. In the first two lists, participants are asked to read respectively
Appendix a set of words for colors that are printed in black ink (List I) and to name
the color of a set of circles (List II). In the third list, color-words are
Cognitive measures printed in an inconsistent color ink (e.g., the word “blue” is printed in
Montreal Cognitive Assessment (MoCA) (Nasreddine et al., 2005). red ink) and participants are required to name the color of the ink, while
Accuracy is collected and a maximal score of 30 can be assigned. The inhibiting reading the word. For each of the 3 tasks, time of completion
final score is then corrected for age and education (Santangelo et al., and accuracy are collected. Both a time interference effect (based on
2015). execution time) and an error interference effect (based on number of
Parkinson’s Disease-Cognitive Rating Scale (PD-CRS) (Santangelo et al., errors) are computed. The final scores are then corrected for age and
2014). The subcortical score (range 0–104) is obtained by adding the education (see Caffarra et al., 2002).
scores of: immediate free-recall verbal memory, sustained attention, “Valutazione delle capacità di costruzione dello scheletro” (Semantic
working memory, unprompted drawing of a clock, delayed free-recall Memory 1 test) and“Denominazione visiva” (Semantic Memory 2 test)
memory, alternating verbal fluency and action verbal fluency. Second, (Sartori & Job, 1988). In the first task, participants are presented with a
the cortical score (range 0–30) is obtained by adding the scores of set of animals and asked to say if the animals are bigger or smaller than a
naming and copy drawing of a clock. Third, the PD-CRS Total score goat. Twenty questions are presented; answers are coded as 1 or 0,
(range 0–134) is obtained by adding the subcortical and cortical scores. respectively for correct and incorrect responses. Afterwards, partici­
The three scores are then corrected for age and education. pants are presented with 20 objects and asked to say if each of these is
Digit Span forward (Monaco et al., 2013; Orsini et al., 1987) Partici­ higher or wider (e.g., ‘is a wardrobe higher or wider?’). Correct answers
pants are read a maximum of 7 lists of digits one at a time and asked to are coded as 1, incorrect answers are coded as 0. The final score is

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M.A. Baraldi et al. Brain and Cognition 150 (2021) 105706

obtained by counting the correct answers, for a maximal score of 40. In Bosco, F. M., Parola, A., Sacco, K., Zettin, M., & Angeleri, R. (2017). Communicative-
pragmatic disorders in traumatic brain injury: The role of theory of mind and
the second task, participants are presented with 64 pictures and asked to
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