Literature DB >> 31235643

The Multiple Representations of Complex Digit Movements in Primary Motor Cortex Form the Building Blocks for Complex Grip Types in Capuchin Monkeys.

Andrei Mayer1, Mary K L Baldwin2, Dylan F Cooke3, Bruss R Lima4, Jeffrey Padberg5, Gabriela Lewenfus4, João G Franca4, Leah Krubitzer6.   

Abstract

In the present study, we investigated motor cortex (M1) and a small portion of premotor and parietal cortex using intracortical microstimulation in anesthetized capuchin monkeys. Capuchins are the only New World monkeys that have evolved an opposable thumb and use tools in the wild. Like most Old World monkeys and humans, capuchin monkeys have highly dexterous hands. We surveyed a large extent of M1 and found that ~22% of all evoked movements in M1 involved the digits, and the majority of these consisted of finger flexions and extensions. Different subtypes of movements could be identified, including opposable movements of digits 1 and 2 (D1 and D2). Interestingly, the pattern of such movements varied between animals. In one case, movements involved the adduction of the medial surface of D1 toward the lateral surface of D2, whereas in the other case, the tips of D1 and D2 came in contact. Unlike other primates examined, we also found extensive representations of the prehensile foot and tail. We propose that the manual behavioral repertoire of capuchin monkeys, which includes the use of tools in the wild, is well represented within the motor cortex in the form of muscle synergies between different body parts that compose these larger, complex behaviors.SIGNIFICANCE STATEMENT The ability to use tools is a milestone in human evolution. Capuchin monkeys are one of the few non-human primates that use tools in the wild. The present study is the first detailed exploration of the motor cortex of these primates using long-train intracortical microstimulation. Within primary motor cortex, we evoked finger movements involving flexions and extensions of multiple digits, or of the first and second digits alone. Interestingly, flexion of tail and toes could also be evoked. Together, these results suggest that the functional organization of the motor cortex represents not just muscles of the body, but muscle synergies that form the building blocks of the complex behavioral repertoire of these animals.
Copyright © 2019 the authors.

Entities:  

Keywords:  finger; grasping; motor cortex; primate

Mesh:

Year:  2019        PMID: 31235643      PMCID: PMC6703879          DOI: 10.1523/JNEUROSCI.0556-19.2019

Source DB:  PubMed          Journal:  J Neurosci        ISSN: 0270-6474            Impact factor:   6.167


  57 in total

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5.  Complex movements evoked by microstimulation of precentral cortex.

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Journal:  Neuron       Date:  2002-05-30       Impact factor: 17.173

6.  Patterns of localization in precentral and "supplementary" motor areas and their relation to the concept of a premotor area.

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7.  Wild capuchin monkeys (Cebus libidinosus) use anvils and stone pounding tools.

Authors:  Dorothy Fragaszy; Patrícia Izar; Elisabetta Visalberghi; Eduardo B Ottoni; Marino Gomes de Oliveira
Journal:  Am J Primatol       Date:  2004-12       Impact factor: 2.371

8.  The ecological role of the prehensile tail in white-faced capuchins (Cebus capucinus).

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9.  Cerebellar loops with motor cortex and prefrontal cortex of a nonhuman primate.

Authors:  Roberta M Kelly; Peter L Strick
Journal:  J Neurosci       Date:  2003-09-10       Impact factor: 6.167

10.  Grasping behavior in tufted capuchin monkeys (Cebus apella): grip types and manual laterality for picking up a small food item.

Authors:  Giovanna Spinozzi; Valentina Truppa; Tiziana Laganà
Journal:  Am J Phys Anthropol       Date:  2004-09       Impact factor: 2.868

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  8 in total

1.  Prehension kinematics in humans and macaques.

Authors:  Yuke Yan; Anton R Sobinov; Sliman J Bensmaia
Journal:  J Neurophysiol       Date:  2022-06-01       Impact factor: 2.974

2.  Coevolution of motor cortex and behavioral specializations associated with flight and echolocation in bats.

Authors:  Andrew C Halley; Mary K L Baldwin; Dylan F Cooke; Mackenzie Englund; Carlos R Pineda; Tobias Schmid; Michael M Yartsev; Leah Krubitzer
Journal:  Curr Biol       Date:  2022-05-25       Impact factor: 10.900

3.  Cortical connectivity is embedded in resting state at columnar resolution.

Authors:  Nicholas S Card; Omar A Gharbawie
Journal:  Prog Neurobiol       Date:  2022-03-12       Impact factor: 10.885

Review 4.  The neural mechanisms of manual dexterity.

Authors:  Anton R Sobinov; Sliman J Bensmaia
Journal:  Nat Rev Neurosci       Date:  2021-10-28       Impact factor: 38.755

5.  Complex tools and motor-to-mechanical transformations.

Authors:  M Ras; M Wyrwa; J Stachowiak; M Buchwald; A M Nowik; G Kroliczak
Journal:  Sci Rep       Date:  2022-05-16       Impact factor: 4.996

6.  Beyond body maps: Information content of specific body parts is distributed across the somatosensory homunculus.

Authors:  Dollyane Muret; Victoria Root; Paulina Kieliba; Danielle Clode; Tamar R Makin
Journal:  Cell Rep       Date:  2022-03-15       Impact factor: 9.423

7.  Moving in on human motor cortex. Characterizing the relationship between body parts with non-rigid population response fields.

Authors:  Wouter Schellekens; Carlijn Bakker; Nick F Ramsey; Natalia Petridou
Journal:  PLoS Comput Biol       Date:  2022-04-04       Impact factor: 4.779

8.  Distributed Motor Control of Limb Movements in Rat Motor and Somatosensory Cortex: The Sensorimotor Amalgam Revisited.

Authors:  Andrew C Halley; Mary K L Baldwin; Dylan F Cooke; Mackenzie Englund; Leah Krubitzer
Journal:  Cereb Cortex       Date:  2020-11-03       Impact factor: 5.357

  8 in total

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