Cortical dynamics and subcortical signatures of motor-language coupling in Parkinson's disease

Margherita Melloni; Lucas Sedeño; Eugenia Hesse; Indira García-Cordero; Ezequiel Mikulan; Angelo Plastino; Aida Marcotti; José David López; Catalina Bustamante; Francisco Lopera; David Pineda; Adolfo M. García; Facundo Manes; Natalia Trujillo; Agustín Ibáñez

doi:10.1038/srep11899

Cortical dynamics and subcortical signatures of motor-language coupling in Parkinson's disease

Margherita Melloni, Lucas Sedeño, Eugenia Hesse, Indira García-Cordero, Ezequiel Mikulan, Angelo Plastino, Aida Marcotti, José David López, Catalina Bustamante, Francisco Lopera, David Pineda, Adolfo M. García, Facundo Manes, Natalia Trujillo, Agustín Ibáñez

School of Psychology

Research output: Contribution to journal › Article › peer-review

66 Scopus citations

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.

Original language	English
Article number	11899
Journal	Scientific Reports
Volume	5
DOIs	https://doi.org/10.1038/srep11899
State	Published - 8 Jul 2015

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Melloni, M., Sedeño, L., Hesse, E., García-Cordero, I., Mikulan, E., Plastino, A., Marcotti, A., López, J. D., Bustamante, C., Lopera, F., Pineda, D., García, A. M., Manes, F., Trujillo, N., & Ibáñez, A. (2015). Cortical dynamics and subcortical signatures of motor-language coupling in Parkinson's disease. Scientific Reports, 5, Article 11899. https://doi.org/10.1038/srep11899

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title = "Cortical dynamics and subcortical signatures of motor-language coupling in Parkinson's disease",

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.",

author = "Margherita Melloni and Lucas Sede{\~n}o and Eugenia Hesse and Indira Garc{\'i}a-Cordero and Ezequiel Mikulan and Angelo Plastino and Aida Marcotti and L{\'o}pez, {Jos{\'e} David} and Catalina Bustamante and Francisco Lopera and David Pineda and Garc{\'i}a, {Adolfo M.} and Facundo Manes and Natalia Trujillo and Agust{\'i}n Ib{\'a}{\~n}ez",

note = "Funding Information: 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.",

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doi = "10.1038/srep11899",

language = "English",

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journal = "Scientific Reports",

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T1 - Cortical dynamics and subcortical signatures of motor-language coupling in Parkinson's disease

AU - Melloni, Margherita

AU - Sedeño, Lucas

AU - Hesse, Eugenia

AU - García-Cordero, Indira

AU - Mikulan, Ezequiel

AU - Plastino, Angelo

AU - Marcotti, Aida

AU - López, José David

AU - Bustamante, Catalina

AU - Lopera, Francisco

AU - Pineda, David

AU - García, Adolfo M.

AU - Manes, Facundo

AU - Trujillo, Natalia

AU - Ibáñez, Agustín

N1 - Funding Information: 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.

PY - 2015/7/8

Y1 - 2015/7/8

N2 - 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.

AB - 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.

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Cortical dynamics and subcortical signatures of motor-language coupling in Parkinson's disease

Abstract

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