Left hemisphere dominance for bilateral kinematic encoding in the human brain.


Journal

eLife
ISSN: 2050-084X
Titre abrégé: Elife
Pays: England
ID NLM: 101579614

Informations de publication

Date de publication:
01 03 2022
Historique:
received: 03 05 2021
accepted: 19 01 2022
entrez: 1 3 2022
pubmed: 2 3 2022
medline: 5 4 2022
Statut: epublish

Résumé

Neurophysiological studies in humans and nonhuman primates have revealed movement representations in both the contralateral and ipsilateral hemispheres. Inspired by clinical observations, we ask if this bilateral representation differs for the left and right hemispheres. Electrocorticography was recorded in human participants during an instructed-delay reaching task, with movements produced with either the contralateral or ipsilateral arm. Using a cross-validated kinematic encoding model, we found stronger bilateral encoding in the left hemisphere, an effect that was present during preparation and was amplified during execution. Consistent with this asymmetry, we also observed better across-arm generalization in the left hemisphere, indicating similar neural representations for right and left arm movements. Notably, these left hemisphere electrodes were centered over premotor and parietal regions. The more extensive bilateral encoding in the left hemisphere adds a new perspective to the pervasive neuropsychological finding that the left hemisphere plays a dominant role in praxis. The brain is split into two hemispheres, each playing the leading role in coordinating movement for the opposite side of the body: lesions on the left hemisphere therefore often result in difficulties moving the right arm or leg, and vice versa. In fact, very few anatomical connections exist between a given hemisphere and the body parts on the same (or ‘ipsilateral’) side. Yet, movements produced with only one limb still engage both sides of the brain, with the hemisphere which does not control the action production, still encoding the direction and speed of the movement. Previous evidence also indicate that the two hemispheres may not have equal roles when coordinating ipsilateral movements. Merrick et al. aimed to shed light on these processes; to do so, they measured electrical activity from the surface of the brain of six patients as they moved their arms to reach a screen. The results revealed that, while the right hemisphere only encoded information about the opposite arm, the left hemisphere contained information about both arms. Finer analyses showed that, for both hemispheres, moving the opposite arm was strongly associated with activity in the primary motor cortex, a region which helps to execute movements. However, in the left hemisphere, movements from the ipsilateral arm were related to activity in brain areas involved in planning and integrating different types of sensory information. These findings contribute to a better understanding of how the motor system works, which could ultimately help with the development of brain-machine interfaces for patients who need a neuroprosthetic limb.

Autres résumés

Type: plain-language-summary (eng)
The brain is split into two hemispheres, each playing the leading role in coordinating movement for the opposite side of the body: lesions on the left hemisphere therefore often result in difficulties moving the right arm or leg, and vice versa. In fact, very few anatomical connections exist between a given hemisphere and the body parts on the same (or ‘ipsilateral’) side. Yet, movements produced with only one limb still engage both sides of the brain, with the hemisphere which does not control the action production, still encoding the direction and speed of the movement. Previous evidence also indicate that the two hemispheres may not have equal roles when coordinating ipsilateral movements. Merrick et al. aimed to shed light on these processes; to do so, they measured electrical activity from the surface of the brain of six patients as they moved their arms to reach a screen. The results revealed that, while the right hemisphere only encoded information about the opposite arm, the left hemisphere contained information about both arms. Finer analyses showed that, for both hemispheres, moving the opposite arm was strongly associated with activity in the primary motor cortex, a region which helps to execute movements. However, in the left hemisphere, movements from the ipsilateral arm were related to activity in brain areas involved in planning and integrating different types of sensory information. These findings contribute to a better understanding of how the motor system works, which could ultimately help with the development of brain-machine interfaces for patients who need a neuroprosthetic limb.

Identifiants

pubmed: 35227374
doi: 10.7554/eLife.69977
pii: 69977
pmc: PMC8887902
doi:
pii:

Types de publication

Journal Article Research Support, N.I.H., Extramural

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : NINDS NIH HHS
ID : R01 NS021135
Pays : United States

Informations de copyright

© 2022, Merrick et al.

Déclaration de conflit d'intérêts

CM, TD, AB, JL, EC, DK, KL, PW, JC, RT No competing interests declared, RI Senior editor, eLife

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Auteurs

Christina M Merrick (CM)

Department of Psychology, University of California, Berkeley, Berkeley, United States.

Tanner C Dixon (TC)

UC Berkeley - UCSF Graduate Program in Bioengineering, University of California, Berkeley, Berkeley, United States.

Assaf Breska (A)

Department of Psychology, University of California, Berkeley, Berkeley, United States.

Jack Lin (J)

Department of Neurology, University of California at Irvine, Irvine, United States.

Edward F Chang (EF)

Department of Neurological Surgery, University of California San Francisco, San Francisco, San Francisco, United States.

David King-Stephens (D)

Department of Neurology and Neurosurgery, California Pacific Medical Center, San Francisco, United States.

Kenneth D Laxer (KD)

Department of Neurology and Neurosurgery, California Pacific Medical Center, San Francisco, United States.

Peter B Weber (PB)

Department of Neurology and Neurosurgery, California Pacific Medical Center, San Francisco, United States.

Jose Carmena (J)

UC Berkeley - UCSF Graduate Program in Bioengineering, University of California, Berkeley, Berkeley, United States.
Department of Electrical Engineering and Computer Sciences, University of California, Berkeley, Berkeley, United States.
Helen Wills Neuroscience Institute, University of California, Berkeley, Berkeley, United States.

Robert Thomas Knight (R)

Department of Psychology, University of California, Berkeley, Berkeley, United States.
UC Berkeley - UCSF Graduate Program in Bioengineering, University of California, Berkeley, Berkeley, United States.
Department of Neurological Surgery, University of California San Francisco, San Francisco, San Francisco, United States.
Helen Wills Neuroscience Institute, University of California, Berkeley, Berkeley, United States.

Richard B Ivry (RB)

Department of Psychology, University of California, Berkeley, Berkeley, United States.
UC Berkeley - UCSF Graduate Program in Bioengineering, University of California, Berkeley, Berkeley, United States.
Helen Wills Neuroscience Institute, University of California, Berkeley, Berkeley, United States.

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