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Gamma-band modulation in the human amygdala during reaching movements

Gogia, Angad S. and Del Campo-Vera, Roberto Martin and Chen, Kuang-Hsuan and Sebastian, Rinu and Nune, George and Kramer, Daniel R. and Lee, Morgan B. and Tafreshi, Ali R. and Barbaro, Michael F. and Liu, Charles Y. and Kellis, Spencer and Lee, Brian (2020) Gamma-band modulation in the human amygdala during reaching movements. Neurosurgical Focus, 49 (1). Art. No. E4. ISSN 1092-0684. https://resolver.caltech.edu/CaltechAUTHORS:20200706-132617645

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Abstract

Objective: Motor brain-computer interface (BCI) represents a new frontier in neurological surgery that could provide significant benefits for patients living with motor deficits. Both the primary motor cortex and posterior parietal cortex have successfully been used as a neural source for human motor BCI, leading to interest in exploring other brain areas involved in motor control. The amygdala is one area that has been shown to have functional connectivity to the motor system; however, its role in movement execution is not well studied. Gamma oscillations (30–200 Hz) are known to be prokinetic in the human cortex, but their role is poorly understood in subcortical structures. Here, the authors use direct electrophysiological recordings and the classic “center-out” direct-reach experiment to study amygdaloid gamma-band modulation in 8 patients with medically refractory epilepsy. Methods: The study population consisted of 8 epilepsy patients (2 men; age range 21–62 years) who underwent implantation of micro-macro depth electrodes for seizure localization and EEG monitoring. Data from the macro contacts sampled at 2000 Hz were used for analysis. The classic center-out direct-reach experiment was used, which consists of an intertrial interval phase, a fixation phase, and a response phase. The authors assessed the statistical significance of neural modulation by inspecting for nonoverlapping areas in the 95% confidence intervals of spectral power for the response and fixation phases. Results: In 5 of the 8 patients, power spectral analysis showed a statistically significant increase in power within regions of the gamma band during the response phase compared with the fixation phase. In these 5 patients, the 95% bootstrapped confidence intervals of trial-averaged power in contiguous frequencies of the gamma band during the response phase were above, and did not overlap with, the confidence intervals of trial-averaged power during the fixation phase. Conclusions: To the authors’ knowledge, this is the first time that direct neural recordings have been used to show gamma-band modulation in the human amygdala during the execution of voluntary movement. This work indicates that gamma-band modulation in the amygdala could be a contributing source of neural signals for use in a motor BCI system.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.3171/2020.4.focus20179DOIArticle
ORCID:
AuthorORCID
Gogia, Angad S.0000-0001-8193-1824
Del Campo-Vera, Roberto Martin0000-0001-9794-2894
Kramer, Daniel R.0000-0003-4551-2977
Lee, Morgan B.0000-0001-6936-0109
Tafreshi, Ali R.0000-0002-8956-3373
Kellis, Spencer0000-0002-5158-1058
Additional Information:© 2020 AANS, except where prohibited by US copyright law. We wish to acknowledge the generous support of the National Center for Advancing Translational Science (NCATS) of the U.S. National Institutes of Health (KL2TR001854), the Tianqiao and Chrissy Chen Brain-Machine Interface Center at Caltech, the Meira and Shaul G. Massry Foundation, and the Taiwan-USC Postdoctoral Fellowship Program. The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper. Author Contributions: Conception and design: Gogia, Martin del Campo-Vera, Chen, Sebastian, Nune, Kramer, Liu, Kellis, B Lee. Acquisition of data: Gogia, Martin del Campo-Vera, Chen, Sebastian, Nune, Kramer, MB Lee, Tafreshi, Barbaro, Kellis, B Lee. Analysis and interpretation of data: Gogia, Martin del Campo-Vera, Chen, Sebastian, Nune, Kramer, MB Lee, Tafreshi, Barbaro, Kellis, B Lee. Drafting the article: Gogia, Martin del Campo-Vera, Chen, Sebastian, Kramer, MB Lee, Tafreshi, Barbaro, Kellis, B Lee. Critically revising the article: all authors. Reviewed submitted version of manuscript: Gogia, Martin del Campo-Vera, Chen, Sebastian, MB Lee, Tafreshi, Barbaro, Liu, Kellis, B Lee. Approved the final version of the manuscript on behalf of all authors: Gogia. Statistical analysis: Gogia, Martin del Campo-Vera, Chen, Sebastian, Kellis, B Lee. Administrative/technical/material support: Nune, Liu, Kellis, B Lee. Study supervision: Nune, Kramer, Liu, Kellis, B Lee.
Group:Tianqiao and Chrissy Chen Institute for Neuroscience
Funders:
Funding AgencyGrant Number
NIHKL2TR001854
Tianqiao and Chrissy Chen Institute for NeuroscienceUNSPECIFIED
Meira and Shaul G. Massry FoundationUNSPECIFIED
Taiwan-USC Postdoctoral Fellowship ProgramUNSPECIFIED
Subject Keywords:gamma band; amygdala; direct reach; stereo-EEG; human; electrophysiology
Issue or Number:1
Record Number:CaltechAUTHORS:20200706-132617645
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20200706-132617645
Official Citation:Gogia, A. S., Martin Del Campo-Vera, R., Chen, K., Sebastian, R., Nune, G., Kramer, D. R., Lee, M. B., Tafreshi, A. R., Barbaro, M. F., Liu, C. Y., Kellis, S., & Lee, B. (2020). Gamma-band modulation in the human amygdala during reaching movements, Neurosurgical Focus FOC, 49(1), E4. Retrieved Jul 6, 2020, from https://thejns.org/focus/view/journals/neurosurg-focus/49/1/article-pE4.xml. doi: 10.3171/2020.4.focus20179
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:104227
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:06 Jul 2020 20:38
Last Modified:16 Nov 2020 23:13

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