Representation of Muscle Synergies in the Primate Brain

Overview

Journal J Neurosci

Specialty Neurology

Date 2015 Sep 18

PMID 26377453

Citations 81

Authors

Simon A Overduin

Andrea dAvella

Jinsook Roh

Jose M Carmena

Emilio Bizzi

Affiliations

Soon will be listed here.

Abstract

Significance Statement: We studied the motor cortical and forearm muscular activity of rhesus macaques (Macaca mulatta) as they reached, grasped, and carried objects of varied shape and size. We applied non-negative matrix factorization separately to the cortical and muscular data to reduce their dimensionality to a smaller set of time-varying "spatiotemporal" synergies. Each synergy represents a sequence of cortical or muscular activity that recurred frequently during the animals' behavior. Salient features of the synergies (including their dimensionality, timing, and amplitude modulation) were observed at both the cortical and muscular levels. The possibility that the brain may execute even complex behaviors using spatiotemporal synergies has implications for neuroprosthetic algorithm design, which could become more computationally efficient by adopting the discrete and low-dimensional control that they afford.

Citing Articles

Exploring Synergies in Brain-Machine Interfaces: Compression vs. Performance.

Cubillos L, Kelberman M, Mender M, Hite A, Temmar H, Willsey M bioRxiv. 2025; .

PMID: 39975237 PMC: 11838491. DOI: 10.1101/2025.02.03.636273.

Quantifying the diverse contributions of hierarchical muscle interactions to motor function.

OReilly D, Shaw W, Hilt P, de Castro Aguiar R, Astill S, Delis I iScience. 2025; 28(1):111613.

PMID: 39834869 PMC: 11742840. DOI: 10.1016/j.isci.2024.111613.

Neuromuscular synergy characteristics of Tai Chi leg stirrup movements: optimal coordination patterns throughout various phases.

Zhang X, Jia M, Ke Y, Zhou J Front Bioeng Biotechnol. 2024; 12:1482793.

PMID: 39506976 PMC: 11538057. DOI: 10.3389/fbioe.2024.1482793.

De novo sensorimotor learning through reuse of movement components.

Gabriel G, Mushtaq F, Morehead J PLoS Comput Biol. 2024; 20(10):e1012492.

PMID: 39388463 PMC: 11495618. DOI: 10.1371/journal.pcbi.1012492.

Variations in Clustering of Multielectrode Local Field Potentials in the Motor Cortex of Macaque Monkeys during a Reach-and-Grasp Task.

Chambellant F, Falaki A, Moreau-Debord I, French R, Serrano E, Quessy S eNeuro. 2024; 11(9).

PMID: 39288997 PMC: 11439563. DOI: 10.1523/ENEURO.0047-24.2024.

References

dAvella A, Portone A, Fernandez L, Lacquaniti F . Control of fast-reaching movements by muscle synergy combinations. J Neurosci. 2006; 26(30):7791-810. PMC: 6674215. DOI: 10.1523/JNEUROSCI.0830-06.2006. View

Graziano M, Taylor C, Moore T . Complex movements evoked by microstimulation of precentral cortex. Neuron. 2002; 34(5):841-51. DOI: 10.1016/s0896-6273(02)00698-0. View

Morrow M, Miller L . Prediction of muscle activity by populations of sequentially recorded primary motor cortex neurons. J Neurophysiol. 2003; 89(4):2279-88. PMC: 2586069. DOI: 10.1152/jn.00632.2002. View

Rathelot J, Strick P . Subdivisions of primary motor cortex based on cortico-motoneuronal cells. Proc Natl Acad Sci U S A. 2009; 106(3):918-23. PMC: 2621250. DOI: 10.1073/pnas.0808362106. View

Overduin S, dAvella A, Carmena J, Bizzi E . Muscle synergies evoked by microstimulation are preferentially encoded during behavior. Front Comput Neurosci. 2014; 8:20. PMC: 3942675. DOI: 10.3389/fncom.2014.00020. View

Cheung V, Piron L, Agostini M, Silvoni S, Turolla A, Bizzi E . Stability of muscle synergies for voluntary actions after cortical stroke in humans. Proc Natl Acad Sci U S A. 2009; 106(46):19563-8. PMC: 2780765. DOI: 10.1073/pnas.0910114106. View

Tresch M, Bizzi E . Responses to spinal microstimulation in the chronically spinalized rat and their relationship to spinal systems activated by low threshold cutaneous stimulation. Exp Brain Res. 1999; 129(3):401-16. DOI: 10.1007/s002210050908. View

Griffin D, Hudson H, Belhaj-Saif A, Cheney P . EMG activation patterns associated with high frequency, long-duration intracortical microstimulation of primary motor cortex. J Neurosci. 2014; 34(5):1647-56. PMC: 3905140. DOI: 10.1523/JNEUROSCI.3643-13.2014. View

dAvella A, Portone A, Lacquaniti F . Superposition and modulation of muscle synergies for reaching in response to a change in target location. J Neurophysiol. 2011; 106(6):2796-812. DOI: 10.1152/jn.00675.2010. View

10.

Stepniewska I, Gharbawie O, Burish M, Kaas J . Effects of muscimol inactivations of functional domains in motor, premotor, and posterior parietal cortex on complex movements evoked by electrical stimulation. J Neurophysiol. 2013; 111(5):1100-19. PMC: 3949230. DOI: 10.1152/jn.00491.2013. View

11.

Schieber M, Rivlis G . Partial reconstruction of muscle activity from a pruned network of diverse motor cortex neurons. J Neurophysiol. 2006; 97(1):70-82. DOI: 10.1152/jn.00544.2006. View

12.

Stark E, Asher I, Abeles M . Encoding of reach and grasp by single neurons in premotor cortex is independent of recording site. J Neurophysiol. 2007; 97(5):3351-64. DOI: 10.1152/jn.01328.2006. View

13.

Flash T, Hochner B . Motor primitives in vertebrates and invertebrates. Curr Opin Neurobiol. 2005; 15(6):660-6. DOI: 10.1016/j.conb.2005.10.011. View

14.

Takei T, Seki K . Spinal interneurons facilitate coactivation of hand muscles during a precision grip task in monkeys. J Neurosci. 2010; 30(50):17041-50. PMC: 6634901. DOI: 10.1523/JNEUROSCI.4297-10.2010. View

15.

Giszter S . Motor primitives--new data and future questions. Curr Opin Neurobiol. 2015; 33:156-65. PMC: 6524953. DOI: 10.1016/j.conb.2015.04.004. View

16.

Santello M, Baud-Bovy G, Jorntell H . Neural bases of hand synergies. Front Comput Neurosci. 2013; 7:23. PMC: 3619124. DOI: 10.3389/fncom.2013.00023. View

17.

Hochberg L, Bacher D, Jarosiewicz B, Masse N, Simeral J, Vogel J . Reach and grasp by people with tetraplegia using a neurally controlled robotic arm. Nature. 2012; 485(7398):372-5. PMC: 3640850. DOI: 10.1038/nature11076. View

18.

Giszter S, Mussa-Ivaldi F, Bizzi E . Convergent force fields organized in the frog's spinal cord. J Neurosci. 1993; 13(2):467-91. PMC: 6576636. View

19.

Ruckert E, dAvella A . Learned parametrized dynamic movement primitives with shared synergies for controlling robotic and musculoskeletal systems. Front Comput Neurosci. 2013; 7:138. PMC: 3797962. DOI: 10.3389/fncom.2013.00138. View

20.

Serruya M, Hatsopoulos N, Paninski L, Fellows M, Donoghue J . Instant neural control of a movement signal. Nature. 2002; 416(6877):141-2. DOI: 10.1038/416141a. View