High-frequency Band Temporal Dynamics in Response to a Grasp Force Task

Overview

Journal J Neural Eng

Specialties Biomedical Engineering
Neurology

Date 2019 Jul 13

PMID 31296796

Citations 3

Authors

Mariana P Branco

Simon H Geukes

Erik J Aarnoutse

Mariska J Vansteensel

Zachary V Freudenburg

Nick F Ramsey

Affiliations

Soon will be listed here.

Abstract

Objective: Brain-computer interfaces (BCIs) are being developed to restore reach and grasping movements of paralyzed individuals. Recent studies have shown that the kinetics of grasping movement, such as grasp force, can be successfully decoded from electrocorticography (ECoG) signals, and that the high-frequency band (HFB) power changes provide discriminative information that contribute to an accurate decoding of grasp force profiles. However, as the models used in these studies contained simultaneous information from multiple spectral features over multiple areas in the brain, it remains unclear what parameters of movement and force are encoded by the HFB signals and how these are represented temporally and spatially in the SMC.

Approach: To investigate this, and to gain insight in the temporal dynamics of the HFB during grasping, we continuously modelled the ECoG HFB response recorded from nine individuals with epilepsy temporarily implanted with ECoG grids, who performed three different grasp force tasks.

Main Results: We show that a model based on the force onset and offset consistently provides a better fit to the HFB power responses when compared with a model based on the force magnitude, irrespective of electrode location.

Significance: Our results suggest that HFB power, although potentially useful for continuous decoding, is more closely related to the changes in movement. This finding may potentially contribute to the more natural decoding of grasping movement in neural prosthetics.

Citing Articles

Behavioral and Neural Variability of Naturalistic Arm Movements.

Peterson S, Singh S, Wang N, Rao R, Brunton B eNeuro. 2021; 8(3).

PMID: 34031100 PMC: 8225404. DOI: 10.1523/ENEURO.0007-21.2021.

Refinement of High-Gamma EEG Features From TBI Patients With Hemicraniectomy Using an ICA Informed by Simulated Myoelectric Artifacts.

Li Y, Wang P, Vaidya M, Flint R, Liu C, Slutzky M Front Neurosci. 2020; 14:599010.

PMID: 33328870 PMC: 7732541. DOI: 10.3389/fnins.2020.599010.

The Representation of Finger Movement and Force in Human Motor and Premotor Cortices.

Flint R, Tate M, Li K, Templer J, Rosenow J, Pandarinath C eNeuro. 2020; 7(4).

PMID: 32769159 PMC: 7438059. DOI: 10.1523/ENEURO.0063-20.2020.

References

Bolu Ajiboye A, Willett F, Young D, Memberg W, Murphy B, Miller J . Restoration of reaching and grasping movements through brain-controlled muscle stimulation in a person with tetraplegia: a proof-of-concept demonstration. Lancet. 2017; 389(10081):1821-1830. PMC: 5516547. DOI: 10.1016/S0140-6736(17)30601-3. 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

Boudreau M, Smith A . Activity in rostral motor cortex in response to predictable force-pulse perturbations in a precision grip task. J Neurophysiol. 2001; 86(3):1079-85. DOI: 10.1152/jn.2001.86.3.1079. View

Hermes D, Siero J, Aarnoutse E, Leijten F, Petridou N, Ramsey N . Dissociation between neuronal activity in sensorimotor cortex and hand movement revealed as a function of movement rate. J Neurosci. 2012; 32(28):9736-44. PMC: 6622254. DOI: 10.1523/JNEUROSCI.0357-12.2012. View

Flint R, Wang P, Wright Z, King C, Krucoff M, Schuele S . Extracting kinetic information from human motor cortical signals. Neuroimage. 2014; 101:695-703. DOI: 10.1016/j.neuroimage.2014.07.049. View

Coon W, Schalk G . A method to establish the spatiotemporal evolution of task-related cortical activity from electrocorticographic signals in single trials. J Neurosci Methods. 2016; 271:76-85. PMC: 5501655. DOI: 10.1016/j.jneumeth.2016.06.024. View

Liu Y, Coon W, de Pesters A, Brunner P, Schalk G . The effects of spatial filtering and artifacts on electrocorticographic signals. J Neural Eng. 2015; 12(5):056008. PMC: 5485665. DOI: 10.1088/1741-2560/12/5/056008. View

Evarts E, Fromm C, Kroller J, Jennings V . Motor Cortex control of finely graded forces. J Neurophysiol. 1983; 49(5):1199-1215. DOI: 10.1152/jn.1983.49.5.1199. View

Branco M, de Boer L, Ramsey N, Vansteensel M . Encoding of kinetic and kinematic movement parameters in the sensorimotor cortex: A Brain-Computer Interface perspective. Eur J Neurosci. 2019; 50(5):2755-2772. PMC: 6625947. DOI: 10.1111/ejn.14342. View

10.

Wessberg J, Stambaugh C, Kralik J, Beck P, Laubach M, Chapin J . Real-time prediction of hand trajectory by ensembles of cortical neurons in primates. Nature. 2000; 408(6810):361-5. DOI: 10.1038/35042582. View

11.

Chen C, Shin D, Watanabe H, Nakanishi Y, Kambara H, Yoshimura N . Decoding grasp force profile from electrocorticography signals in non-human primate sensorimotor cortex. Neurosci Res. 2014; 83:1-7. DOI: 10.1016/j.neures.2014.03.010. View

12.

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

13.

Crone N, Miglioretti D, Gordon B, Lesser R . Functional mapping of human sensorimotor cortex with electrocorticographic spectral analysis. II. Event-related synchronization in the gamma band. Brain. 1999; 121 ( Pt 12):2301-15. DOI: 10.1093/brain/121.12.2301. View

14.

Evarts E . Relation of pyramidal tract activity to force exerted during voluntary movement. J Neurophysiol. 1968; 31(1):14-27. DOI: 10.1152/jn.1968.31.1.14. View

15.

Cheney P, Fetz E . Functional classes of primate corticomotoneuronal cells and their relation to active force. J Neurophysiol. 1980; 44(4):773-91. DOI: 10.1152/jn.1980.44.4.773. View

16.

Branco M, Gaglianese A, Glen D, Hermes D, Saad Z, Petridou N . ALICE: A tool for automatic localization of intra-cranial electrodes for clinical and high-density grids. J Neurosci Methods. 2017; 301:43-51. PMC: 5952625. DOI: 10.1016/j.jneumeth.2017.10.022. View

17.

Georgopoulos A, Kalaska J, Caminiti R, Massey J . On the relations between the direction of two-dimensional arm movements and cell discharge in primate motor cortex. J Neurosci. 1982; 2(11):1527-37. PMC: 6564361. View

18.

Smith A, Hepp-Reymond M, Wyss U . Relation of activity in precentral cortical neurons to force and rate of force change during isometric contractions of finger muscles. Exp Brain Res. 1975; 23(3):315-32. DOI: 10.1007/BF00239743. View

19.

Pistohl T, Schulze-Bonhage A, Aertsen A, Mehring C, Ball T . Decoding natural grasp types from human ECoG. Neuroimage. 2011; 59(1):248-60. DOI: 10.1016/j.neuroimage.2011.06.084. View

20.

Salari E, Freudenburg Z, Vansteensel M, Ramsey N . Spatial-Temporal Dynamics of the Sensorimotor Cortex: Sustained and Transient Activity. IEEE Trans Neural Syst Rehabil Eng. 2018; 26(5):1084-1092. PMC: 6080691. DOI: 10.1109/TNSRE.2018.2821058. View