Action-type mapping principles extend beyond evolutionarily conserved actions, even in people born without hands

How are actions represented in the motor system? Although the sensorimotor system is broadly organized somatotopically, higher-level sensorimotor areas encode action-type information for reaching and grasping actions-regardless of the acting body part. Does the brain similarly support generalization across acting body parts for more evolutionarily recent actions, such as tool-use? We tested whether there is a body-part-independent action-type organization in sensorimotor areas by examining fMRI responses for tool-use actions that participants performed with their hands or feet. We additionally included individuals born without hands to test whether hand sensorimotor experience is necessary for the development of this action-type organization. Across analyses, we found a consistent dissociation in the motor system. The primary sensorimotor cortices encoded concrete, body-part specific information in both groups. In contrast, higher-level motor areas within the tool-use network represent abstract, action-type information independent of the body part for both groups. Together, our results suggest that the hierarchical organization of the motor system is not dependent on a long evolutionary history of an action. Further, this organization is not dependent on an individual's manual sensorimotor experience. Our results also show that the functional reorganization in congenital handlessness follows the hierarchical organization of the intact cortex, revealing the limitations of brain plasticity. Finally, the results support using a readout of a more abstract code for hierarchical brain-computer interfaces.

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Publication Details

Journal
Proceedings of the National Academy of Sciences
Published
2025-08-19
DOI
https://doi.org/10.1073/pnas.2503188122
Citations
3
Primary Topic
Action Observation and Synchronization
Type
article
Field-Weighted Citation Impact
7.32
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article

Action-type mapping principles extend beyond evolutionarily conserved actions, even in people born without hands

Ella Striem-Amit, Jody C. Culham, Kibong Moon, Lénia Amaral et al.
3 citations
Proceedings of the National Academy of Sciences
Action Observation and Synchronization
7.32
article

Action-type mapping principles extend beyond evolutionarily conserved actions, even in people born without hands

Ella Striem-Amit, Jody C. Culham, Kibong Moon, Lénia Amaral, Florencia Martinez Addiego, Sriparna Sen, Maximilian Riesenhuber, Yuqi Liu, Caroline O’Brien, Elizabeth Shytle
article en
3 citations

Abstract

How are actions represented in the motor system? Although the sensorimotor system is broadly organized somatotopically, higher-level sensorimotor areas encode action-type information for reaching and grasping actions-regardless of the acting body part. Does the brain similarly support generalization across acting body parts for more evolutionarily recent actions, such as tool-use? We tested whether there is a body-part-independent action-type organization in sensorimotor areas by examining fMRI responses for tool-use actions that participants performed with their hands or feet. We additionally included individuals born without hands to test whether hand sensorimotor experience is necessary for the development of this action-type organization. Across analyses, we found a consistent dissociation in the motor system. The primary sensorimotor cortices encoded concrete, body-part specific information in both groups. In contrast, higher-level motor areas within the tool-use network represent abstract, action-type information independent of the body part for both groups. Together, our results suggest that the hierarchical organization of the motor system is not dependent on a long evolutionary history of an action. Further, this organization is not dependent on an individual's manual sensorimotor experience. Our results also show that the functional reorganization in congenital handlessness follows the hierarchical organization of the intact cortex, revealing the limitations of brain plasticity. Finally, the results support using a readout of a more abstract code for hierarchical brain-computer interfaces.

Proceedings of the National Academy of SciencesVol. 122(34)
Western University (CA), University of Pittsburgh (US), Georgetown University (US), Georgetown University Medical Center (US), Center for Excellence in Brain Science and Intelligence Technology (CN), Center for Neuro-Oncology (US), University of Coimbra (PT)
Openalex Percentile: Top 3%
Action Observation and Synchronization
7.32
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