Elsevier

Cortex

Volume 69, August 2015, Pages 237-254
Cortex

Research report
Syntax, action verbs, action semantics, and object semantics in Parkinson's disease: Dissociability, progression, and executive influences

https://doi.org/10.1016/j.cortex.2015.05.022Get rights and content

Abstract

Several studies have recently shown that basal ganglia (BG) deterioration leads to distinctive impairments in the domains of syntax, action verbs, and action semantics. In particular, such disruptions have been repeatedly observed in Parkinson's disease (PD) patients. However, it remains unclear whether these deficits are language-specific and whether they are equally dissociable from other reported disturbances –viz., processing of object semantics. To address these issues, we administered linguistic, semantic, and executive function (EFs) tasks to two groups of non-demented PD patients, with and without mild cognitive impairment (PD-MCI and PD-nMCI, respectively). We compared these two groups with each other and with matched samples of healthy controls. Our results showed that PD patients exhibited linguistic and semantic deficits even in the absence of MCI. However, not all domains were equally related to EFs and MCI across samples. Whereas EFs predicted disturbances of syntax and object semantics in both PD-nMCI and PD-MCI, they had no impact on action-verb and action-semantic impairments in either group. Critically, patients showed disruptions of action-verb production and action semantics in the absence of MCI and without any executive influence, suggesting a sui generis deficit present since early stages of the disease. These findings indicate that varied language domains are differentially related to the BG, contradicting popular approaches to neurolinguistics.

Introduction

A massive body of evidence gathered in the last fifteen years indicates that high-order cognition is rooted in lower-level sensorimotor systems. This view, which lies at the core of the embodied cognition framework (e.g., Barsalou, 1999, Gallese and Lakoff, 2005), has inspired novel approaches to the study of language. In short, the underlying question is whether language-specific distinctions (for example, at the semantic and lexical levels) are grounded in non-verbal perceptual and motor mechanisms.

Several reports have demonstrated distinctive associations between varied noun types and relevant perceptual systems. For example, Gonzalez et al. (2006) observed that odor-related words, as opposed to odor-neutral terms, activate smell-related structures in the primary olfactory cortex. Similarly, noun comprehension has been shown to rapidly activate modality-specific networks supporting shape (Wheatley, Weisberg, Beauchamp, & Martin, 2005) and color (Simmons et al., 2007) perception.

Even more studies have focused on the relationship between motor skills and language processing. In particular, researchers from varied fields have used linguistic tasks to examine referential motor resonance, namely, the relationship between the contents of verbal stimuli and relevant motor circuitry (Fischer & Zwaan, 2008). Of particular importance to this line of research is the study of linguistic and semantic skills in Parkinson's disease (PD), the second most prevalent neurodegenerative disorder worldwide (Tanner & Goldman, 1996). Available findings are highly relevant to constrain neurolinguistic models, establish early markers of the disease, and delineate therapeutic programs (García & Ibáñez, 2014). However, critical questions remain unanswered regarding the nature, dissociability, and progression of linguistic and semantic impairments in this population. The exploration of these issues could be used to constrain models of language embodiment and eventually hone their clinical relevance.

PD is associated with basal ganglia (BG) dysfunction, resulting from progressive degeneration of dopaminergic neurons projecting from the substantia nigra to striatal motor loci (Fearnley and Lees, 1991, Rodriguez-Oroz et al., 2009). Its main clinical feature is the loss of voluntary movement control, including resting tremor, postural instability, and bradykinesia (Helmich et al., 2012, Liu et al., 2006, Rosin et al., 1997). In addition to motor symptoms, PD involves deficits in high-order cognitive domains, such as attention, working memory (WM), and other executive functions (EFs) (Dubois and Pillon, 1996, Green et al., 2002, Hochstadt et al., 2006). Furthermore, from early stages of the disease, patients manifest dysfunctions in two specific linguistic domains: syntax and action verbs (the latter at both the lexical and the semantic levels).

First, PD patients are impaired in processing sentences of varied syntactic complexity, as observed in both monolingual (Lee et al., 2003, Lieberman et al., 1992) and bilingual (Zanini et al., 2004) samples. Such deficits seem to be task-independent, as they were separately observed in self-paced reading, auditory comprehension (Angwin, Chenery, Copland, Murdoch, & Silburn, 2006), and sentence-picture matching (Hochstadt et al., 2006) tasks. Syntactic affectations in PD patients have been associated with abnormal P600 modulations (Friederici, Kotz, Werheid, Hein, & von Cramon, 2003) and reduced activations in bilateral fronto-temporal and striatal sites (Grossman et al., 2003).

Second, PD involves marked deficits in action verbs with relative preservation of noun processing. This was shown in tasks tapping semantic and/or lexical processes, such as object versus action picture naming (Bertella et al., 2002, Herrera and Cuetos, 2012, Rodriguez-Ferreiro et al., 2009), related-word production (Peran et al., 2003), and lexical decision (Boulenger et al., 2008). Moreover, when the production of both action verbs and nouns is affected in PD, deficits are larger in the former word class (Cotelli et al., 2007, Crescentini et al., 2008). Strikingly, action-verb processing may be compromised even when abstract verbs are spared (Fernandino et al., 2013). High-order deficits involving action-related information in PD have also been revealed at a strictly semantic level, through picture-association tasks (Ibáñez et al., 2013). The latter paradigms are useful to disentangle conceptual and lexical factors in the observed deficits (see Vigliocco, Vinson, Druks, Barber, & Cappa, 2011), as semantic representations of pictures can be presumed to largely overlap with those evoked by their verbal labels (Bak & Hodges, 2003). Neural correlates of impaired action-verb processing in PD involve aberrant frontotemporal connectivity (Melloni et al., 2015) and damage to a BG-cortico-subcortical motor network (Cardona et al., 2014), including the prefrontal cortex, Brocaʼs area, and the anterior cingulate cortex (Péran et al., 2009), and the subthalamic nucleus (Silveri et al., 2012).

Taken together, the above findings indicate that syntax, action verbs, and action semantics are specifically compromised in PD. Thus, BG circuits seem to be key components of the networks underlying these domains, as observed in clinical (Murray, 2000, Teichmann et al., 2008, Teichmann et al., 2005) and neurotypical (Moro et al., 2001) samples. The role of BG in syntactic processing has been proposed to reflect their specialization for the acquisition and execution of hierarchical and sequential motor/cognitive routines (Ullman, 2001), their role in EFs (Grossman, 1999, Grossman et al., 2002a, Grossman et al., 2002b, Lee et al., 2003), and their involvement in cue-guided predictions (Kotz, Schwartze, & Schmidt-Kassow, 2009). Similarly, the crucial engagement of frontobasal structures during action-verb processing is highlighted by selective semantic and lexical deficits observed in multiple neurodegenerative motor diseases, such as motor neuron disease (Bak, 2013, Bak and Hodges, 2004, Bak et al., 2001, Bak et al., 2006, Hodges and Bak, 1997), amyotrophic lateral sclerosis (Bak and Hodges, 2004, Neary et al., 2000), progressive supranuclear palsy (Bak et al., 2001, Bak et al., 2006), corticobasal degeneration (Cotelli et al., 2006, Silveri and Ciccarelli, 2007), and Huntingtonʼs disease (Kargieman et al., 2014).

The role of the BG in action-verb processing supports embodied approaches to cognitive modeling. For example, Cardona et al. (2013) and Ibáñez et al. (2013) postulate that action-verb processing and motor-language coupling depend on a network involving loops from cortical areas to BG/thalamic structures and back to the cortex. Hence, BG affectation in early PD would lead to the selective disruption of this language domain.

Note, at this juncture, that virtually all studies on language processing in PD have been conducted with non-demented patients (Bertella et al., 2002, Boulenger et al., 2008, Cotelli et al., 2007, Grossman et al., 1992, Grossman et al., 2003, Herrera and Cuetos, 2012, Lieberman et al., 1990, Lieberman et al., 1992). However, recent clinical research demonstrates that PD patients can manifest cognitive impairment even without reaching levels of dementia. Such a stage is known as mild cognitive impairment (MCI) (Aarsland et al., 2010, Caviness et al., 2007, Janvin et al., 2006, Litvan et al., 2011, Yu et al., 2012). Prospective studies suggest that a considerable percentage of PD patients without cognitive impairment develop MCI just a few years after diagnosis (Broeders et al., 2013, Hobson and Meara, 2015). Following the onset of MCI, PD patients have a higher risk of developing dementia (Aarsland et al., 2003, Buter et al., 2008, Janvin et al., 2005, Reid et al., 2011, Williams-Gray et al., 2013). These findings indicate that the course of PD involves continuum that goes from normal cognition to MCI to dementia. Consequently, the difference between absence and presence of MCI can be taken as a proxy of disease progression.

These prolegomena motivate three important questions regarding syntactic, action-verb, and action-semantic skills in PD and their relation to EFs and MCI. First, is the affectation of these skills domain-specific, or does it depend on executive or otherwise cognitive impairment? Second, is their disturbance equally dissociable from other deficits (viz., processing of object semantics)? Third, do such potential relationships vary as cognitive impairment worsens throughout the course of disease?

Whereas the latter two questions have not been directly assessed in the literature, the first one has yielded contradictory views. Some authors contend that syntactic deficits in PD are epiphenomenal to executive dysfunction (Angwin et al., 2006, Hochstadt et al., 2006, Longworth et al., 2005) or impairments of selective attention (Lee et al., 2003). In a similar vein, action-verb deficits in PD have been attributed to underlying inhibitory control (Copland, 2003) or WM (Colman et al., 2009) deficits. However, the non-demented PD patients tested by Rodriguez-Ferreiro et al. (2009) exhibited significant impairments in action (but not in object) naming without concurrent executive impairment. Similarly, the early PD patients assessed by Ibáñez et al. (2013) evinced deficits in both action semantics and the ability to integrate action-verb and motor information, but these deficits were not associated with executive or general cognitive impairment.

The above questions give rise to distinct empirical predictions. First, following Rodriguez-Ferreiro et al. (2009) and Ibáñez et al. (2013), such linguistic deficits should not be caused by executive dysfunction. Second, if they are secondary to overall cognitive deficits, they should be absent in patients without MCI. Finally, if they are distinctively sui generis, they should differentially occur independently of MCI and executive dysfunction –the same should not be the case for deficits in non-action-related domains, such as object semantics.

To test such predictions, we assessed syntax, action verbs, action semantics, object semantics, and EFs in two patient groups: PD patients with and without MCI (PD-MCI and PD-nMCI, respectively). This way, we examine the dissociability and progression of linguistic and semantic disturbances in PD and their relation with executive performance and MCI.

Section snippets

Participants

Forty non-demented PD patients and 40 healthy volunteers participated in this study. Clinical diagnosis of PD was made by two neurologists (B.O. and V.A.) in accordance with the United Kingdom PD Society Brain Bank criteria (Hughes, Daniel, Kilford, & Lees, 1992). Motor impairments were assessed with the motor section of the Unified Parkinson's Disease Rating Scale (UPDRS) (Fahn & Elton, 1987). Disease stage was rated with the Hoehn & Yahr scale (H&Y) (Hoehn & Yahr, 1967). All the patients were

Demographic data and clinical evaluation

The control group and the PD patients were similar in age [t (78) = −.65, p = .51], education level [t (78) = .75, p = .45], and gender [χ2 (1) = .05, p = .82]. Relative to their corresponding control subgroups, neither PD-nMCI nor PD-MCI showed significant differences in age [t (44) = −.49, p = .62, and t (32) = −.46, p = .65, respectively] and education level [U = 258.5, p = .89, and U = 131.5, p = .65, respectively]. The PD-nMCI and PD-MCI groups did not differ significantly in terms of age [

Are linguistic and semantic deficits predicted by executive impairment?

We estimated different models in which each language measure was separately considered as a dependent variable while the total IFS score (indexing EF skills) was framed as a predictor. In a subsequent analysis, the group variable (nMCI, MCI) was also introduced as a second predictor. For further data, see Table 3.

Discussion

The present study examined the dissociability and progression of linguistic and semantic deficits in PD and their relation with EFs. To this end, we administered syntactic, action-naming, semantic association, and executive tasks to two samples of non-demented PD patients differing in their level of cognitive impairment (PD-nMCI and PD-MCI). We compared these two groups with each other and with matched samples of healthy controls. In particular, we explored whether linguistic and semantic

Conclusions

To summarize, different linguistic and semantic domains are significantly impaired in PD, even in the absence of MCI. Our findings indicate that action-naming and action-semantic deficits in this population constitute a sui generis disturbance, whereas impairments of syntax and object semantics are secondary to executive dysfunction. Also, the present data support an embodied cognition model in which a BG-cortical network involving a motor circuit and a semantic circuit proves critical for

Acknowledgments

This work was partially supported by grants from CONICET, CONICYT/FONDECYT Regular (1130920), COLCIENCIAS (1115-545-31374 and 1115-569-33858), FONCyT-PICT 2012-0412, FONCyT-PICT 2012-1309, and the INECO Foundation. We thank Jorge Rendon and Aracelly Castro for their contribution with the medical and cognitive evaluations.

References (126)

  • A. Daniele et al.

    Selective impairment of action-verb naming and comprehension in progressive supranuclear palsy

    Cortex

    (2013)
  • L. Fernandino et al.

    Parkinson's disease disrupts both automatic and controlled processing of action verbs

    Brain Lang

    (2013)
  • J. Gonzalez et al.

    Reading cinnamon activates olfactory brain regions

    NeuroImage

    (2006)
  • M. Grossman

    Sentence processing in Parkinson's disease

    Brain Cogn

    (1999)
  • M. Grossman et al.

    Sentence comprehension in Parkinson's disease: the role of attention and memory

    Brain Lang

    (1992)
  • M. Grossman et al.

    Assessing resource demands during sentence processing in Parkinson's disease

    Brain Lang

    (2002)
  • S.N. Haber et al.

    The cortico-basal ganglia integrative network: the role of the thalamus

    Brain Research Bulletin

    (2009)
  • E. Herrera et al.

    Action naming in Parkinson's disease patients on/off dopamine

    Neuroscience Letters

    (2012)
  • J. Hochstadt et al.

    The roles of sequencing and verbal working memory in sentence comprehension deficits in Parkinson's disease

    Brain Lang

    (2006)
  • A. Ibáñez et al.

    Motor-language coupling: direct evidence from early Parkinson's disease and intracranial cortical recordings

    Cortex

    (2013)
  • P.J. James et al.

    Working memory predicts semantic comprehension in dichotic listening in older adults

    Cognition

    (2014)
  • E. Jefferies

    The neural basis of semantic cognition: converging evidence from neuropsychology, neuroimaging and TMS

    Cortex

    (2013)
  • S.A. Kotz et al.

    Non-motor basal ganglia functions: a review and proposal for a model of sensory predictability in auditory language perception

    Cortex

    (2009)
  • C. Lee et al.

    Attentional resource and processing speed limitations during sentence processing in Parkinson's disease

    Brain Lang

    (2003)
  • S.E. Leh et al.

    Fronto-striatal connections in the human brain: a probabilistic diffusion tractography study

    Neuroscience Letters

    (2007)
  • E. Lepron et al.

    A PET study of word generation in Huntington's disease: effects of lexical competition and verb/noun category

    Brain Lang

    (2009)
  • P. Lieberman et al.

    Speech production, syntax comprehension, and cognitive deficits in Parkinson's disease

    Brain Lang

    (1992)
  • W. Liu et al.

    Bilateral subthalamic stimulation improves gait initiation in patients with Parkinson's disease

    Gait & Posture

    (2006)
  • B.F. Marino et al.

    Language sensorimotor specificity modulates the motor system

    Cortex

    (2012)
  • A. Moro et al.

    Syntax and the brain: disentangling grammar by selective anomalies

    NeuroImage

    (2001)
  • D. Neary et al.

    Cognitive change in motor neurone disease/amyotrophic lateral sclerosis (MND/ALS)

    Journal of the Neurological Sciences

    (2000)
  • P. Péran et al.

    Object naming and action-verb generation in Parkinson's disease: a fMRI study

    Cortex

    (2009)
  • D. Aarsland et al.

    Prevalence and characteristics of dementia in Parkinson disease: an 8-year prospective study

    Archives of Neurology

    (2003)
  • D. Aarsland et al.

    Cognitive impairment in incident, untreated Parkinson disease: the Norwegian ParkWest study

    Neurology

    (2009)
  • D. Aarsland et al.

    Mild cognitive impairment in Parkinson disease: a multicenter pooled analysis

    Neurology

    (2010)
  • P. Aravena et al.

    Action relevance in linguistic context drives word-induced motor activity

    Frontiers in Human Neuroscience

    (2014)
  • T.H. Bak

    The neuroscience of action semantics in neurodegenerative brain diseases

    Current Opinion In Neurology

    (2013)
  • T.H. Bak et al.

    Selective impairment of verb processing associated with pathological changes in Brodmann areas 44 and 45 in the motor neurone disease-dementia-aphasia syndrome

    Brain

    (2001)
  • T.H. Bak et al.

    Clinical, imaging and pathological correlates of a hereditary deficit in verb and action processing

    Brain

    (2006)
  • L.W. Barsalou

    Perceptual symbol systems

    Behavioral and Brain Sciences

    (1999)
  • L. Bertella et al.

    Noun verb dissociation in Parkinson's disease

    Brain Cogn

    (2002)
  • M. Broeders et al.

    Evolution of mild cognitive impairment in Parkinson disease

    Neurology

    (2013)
  • K. Bronnick et al.

    Profile of cognitive impairment in dementia associated with Parkinson's disease compared with Alzheimer's disease

    Journal of Neurology, Neurosurgery, and Psychiatry

    (2007)
  • T.C. Buter et al.

    Dementia and survival in Parkinson disease: a 12-year population study

    Neurology

    (2008)
  • J.F. Cardona et al.

    Action-verb processing in Parkinson's disease: new pathways for motor-language coupling

    Brain Struct Funct

    (2013)
  • J. Cardona et al.

    How embodied is action language? Neurological evidence from motor diseases

    Cognition

    (2014)
  • J.N. Caviness et al.

    Defining mild cognitive impairment in Parkinson's disease

    Movement Disorders

    (2007)
  • K.S. Colman et al.

    Sentence comprehension and its association with executive functions in patients with Parkinson's disease

    Parkinson's Disease

    (2011)
  • D. Copland

    The basal ganglia and semantic engagement: potential insights from semantic priming in individuals with subcortical vascular lesions, Parkinson's disease, and cortical lesions

    Journal of the International Neuropsychological Society

    (2003)
  • M. Cotelli et al.

    Action and object naming in frontotemporal dementia, progressive supranuclear palsy, and corticobasal degeneration

    Neuropsychology

    (2006)
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