Decoding Grasp and Speech Signals from the Cortical Grasp Circuit in a Tetraplegic Human

Overview

Journal Neuron

Publisher Cell Press

Specialty Neurology

Date 2022 Apr 1

PMID 35364014

Authors

Sarah K Wandelt

Spencer Kellis

David A Bjanes

Kelsie Pejsa

Brian Lee

Charles Liu

Richard A Andersen

Affiliations

Soon will be listed here.

Abstract

The cortical grasp network encodes planning and execution of grasps and processes spoken and written aspects of language. High-level cortical areas within this network are attractive implant sites for brain-machine interfaces (BMIs). While a tetraplegic patient performed grasp motor imagery and vocalized speech, neural activity was recorded from the supramarginal gyrus (SMG), ventral premotor cortex (PMv), and somatosensory cortex (S1). In SMG and PMv, five imagined grasps were well represented by firing rates of neuronal populations during visual cue presentation. During motor imagery, these grasps were significantly decodable from all brain areas. During speech production, SMG encoded both spoken grasp types and the names of five colors. Whereas PMv neurons significantly modulated their activity during grasping, SMG's neural population broadly encoded features of both motor imagery and speech. Together, these results indicate that brain signals from high-level areas of the human cortex could be used for grasping and speech BMI applications.

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References

Osiurak F, Badets A . Tool use and affordance: Manipulation-based versus reasoning-based approaches. Psychol Rev. 2016; 123(5):534-68. DOI: 10.1037/rev0000027. View

Wilson G, Stavisky S, Willett F, Avansino D, Kelemen J, Hochberg L . Decoding spoken English from intracortical electrode arrays in dorsal precentral gyrus. J Neural Eng. 2020; 17(6):066007. PMC: 8293867. DOI: 10.1088/1741-2552/abbfef. View

McDowell T, Holmes N, Sunderland A, Schurmann M . TMS over the supramarginal gyrus delays selection of appropriate grasp orientation during reaching and grasping tools for use. Cortex. 2018; 103:117-129. DOI: 10.1016/j.cortex.2018.03.002. View

Hecht M, Hillemacher T, Grasel E, Tigges S, Winterholler M, Heuss D . Subjective experience and coping in ALS. Amyotroph Lateral Scler Other Motor Neuron Disord. 2003; 3(4):225-31. DOI: 10.1080/146608202760839009. View

Branco M, Freudenburg Z, Aarnoutse E, Bleichner M, Vansteensel M, Ramsey N . Decoding hand gestures from primary somatosensory cortex using high-density ECoG. Neuroimage. 2016; 147:130-142. PMC: 5322832. DOI: 10.1016/j.neuroimage.2016.12.004. View

Collinger J, Wodlinger B, Downey J, Wang W, Tyler-Kabara E, Weber D . High-performance neuroprosthetic control by an individual with tetraplegia. Lancet. 2012; 381(9866):557-64. PMC: 3641862. DOI: 10.1016/S0140-6736(12)61816-9. View

Orban G, Caruana F . The neural basis of human tool use. Front Psychol. 2014; 5:310. PMC: 3988392. DOI: 10.3389/fpsyg.2014.00310. View

Garcea F, Buxbaum L . Gesturing tool use and tool transport actions modulates inferior parietal functional connectivity with the dorsal and ventral object processing pathways. Hum Brain Mapp. 2019; 40(10):2867-2883. PMC: 6548598. DOI: 10.1002/hbm.24565. View

Potok W, Maskiewicz A, Kroliczak G, Marangon M . The temporal involvement of the left supramarginal gyrus in planning functional grasps: A neuronavigated TMS study. Cortex. 2018; 111:16-34. DOI: 10.1016/j.cortex.2018.10.010. View

10.

Stoeckel C, Gough P, Watkins K, Devlin J . Supramarginal gyrus involvement in visual word recognition. Cortex. 2009; 45(9):1091-6. PMC: 2726132. DOI: 10.1016/j.cortex.2008.12.004. View

11.

Sakata H, Taira M, Murata A, Mine S . Neural mechanisms of visual guidance of hand action in the parietal cortex of the monkey. Cereb Cortex. 1995; 5(5):429-38. DOI: 10.1093/cercor/5.5.429. View

12.

Klaes C, Kellis S, Aflalo T, Lee B, Pejsa K, Shanfield K . Hand Shape Representations in the Human Posterior Parietal Cortex. J Neurosci. 2015; 35(46):15466-76. PMC: 4649012. DOI: 10.1523/JNEUROSCI.2747-15.2015. View

13.

Oberhuber M, Hope T, Seghier M, Parker Jones O, Prejawa S, Green D . Four Functionally Distinct Regions in the Left Supramarginal Gyrus Support Word Processing. Cereb Cortex. 2016; 26(11):4212-4226. PMC: 5066832. DOI: 10.1093/cercor/bhw251. View

14.

Styrkowiec P, Nowik A, Kroliczak G . The neural underpinnings of haptically guided functional grasping of tools: An fMRI study. Neuroimage. 2019; 194:149-162. DOI: 10.1016/j.neuroimage.2019.03.043. View

15.

Taira M, Mine S, Georgopoulos A, Murata A, Sakata H . Parietal cortex neurons of the monkey related to the visual guidance of hand movement. Exp Brain Res. 1990; 83(1):29-36. DOI: 10.1007/BF00232190. View

16.

Schaffelhofer S, Scherberger H . Object vision to hand action in macaque parietal, premotor, and motor cortices. Elife. 2016; 5. PMC: 4961460. DOI: 10.7554/eLife.15278. View

17.

Gallivan J, McLean D, Valyear K, Culham J . Decoding the neural mechanisms of human tool use. Elife. 2013; 2:e00425. PMC: 3667577. DOI: 10.7554/eLife.00425. View

18.

Reynaud E, Navarro J, Lesourd M, Osiurak F . To Watch is to Work: a Review of NeuroImaging Data on Tool Use Observation Network. Neuropsychol Rev. 2019; 29(4):484-497. DOI: 10.1007/s11065-019-09418-3. View

19.

Bashford L, Rosenthal I, Kellis S, Pejsa K, Kramer D, Lee B . The Neurophysiological Representation of Imagined Somatosensory Percepts in Human Cortex. J Neurosci. 2021; 41(10):2177-2185. PMC: 8018772. DOI: 10.1523/JNEUROSCI.2460-20.2021. View

20.

Anderson K . Targeting recovery: priorities of the spinal cord-injured population. J Neurotrauma. 2005; 21(10):1371-83. DOI: 10.1089/neu.2004.21.1371. View