Abstract
Impairments of action language have been documented in early stage Parkinson’s disease (EPD). The action-sentence compatibility effect (ACE) paradigm has revealed that EPD involves deficits to integrate action-verb processing and ongoing motor actions. Recent studies suggest that an abolished ACE in EPD reflects a cortico-subcortical disruption, and recent neurocognitive models highlight the role of the basal ganglia (BG) in motor-language coupling. Building on such breakthroughs, we report the first exploration of convergent cortical and subcortical signatures of ACE in EPD patients and matched controls. Specifically, we combined cortical recordings of the motor potential, functional connectivity measures, and structural analysis of the BG through voxel-based morphometry. Relative to controls, EPD patients exhibited an impaired ACE, a reduced motor potential, and aberrant frontotemporal connectivity. Furthermore, motor potential abnormalities during the ACE task were predicted by overall BG volume and atrophy. These results corroborate that motor-language coupling is mainly subserved by a cortico-subcortical network including the BG as a key hub. They also evince that action-verb processing may constitute a neurocognitive marker of EPD. Our findings suggest that research on the relationship between language and motor domains is crucial to develop models of motor cognition as well as diagnostic and intervention strategies.
Highlights
Across compatible and incompatible trials[9,10,11,12]
Our results showed that early stages of PD (EPD) patients exhibited (a) behavioral impairments in the action-sentence compatibility effect (ACE) task, accompanied by (b) a reduced cortical motor potential (MP) and (c) aberrant frontotemporal network activity
Multiple reports in the last two decades have indicated that impairments of movement and cognition are not separate phenomena[38,39]
Summary
Across compatible and incompatible trials[9,10,11,12]. The ACE is defined as shorter reaction times in compatible conditions (namely, when the action denoted by a verb involves a hand position similar to the one used to press the response button). Motor-language coupling deficits in PD seem to result from damage to a BG-cortical motor network involving loops from frontotemporal areas to BG/thalamic structures and back to the cortex[3,14,16]. According to this model, BG impairment would disturb processing in this cortico-subcortical motor network, leading to action-verb deficits in EPD patients. The above evidence suggests that action-language deficits in EPD involve multilevel disruptions in cortico-subcortical motor networks To explore this possibility, we administered the ACE task to a group of EPD patients and examined potential cortical and subcortical markers of impaired performance. Through this multi-dimensional approach, we offer unprecedented evidence of electrophysiological and structural signatures of ACE performance in EPD
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