Neural population dynamics reveals disruption of spinal circuits' responses to proprioceptive input during electrical stimulation of sensory afferents.

CP: Neuroscience electrical stimulation manifold neural population dynamics somatosensory cortex spinal cord spinal sensorimotor computations

Journal

Cell reports
ISSN: 2211-1247
Titre abrégé: Cell Rep
Pays: United States
ID NLM: 101573691

Informations de publication

Date de publication:
19 Jan 2024
Historique:
received: 30 05 2023
revised: 08 11 2023
accepted: 06 01 2024
medline: 21 1 2024
pubmed: 21 1 2024
entrez: 21 1 2024
Statut: aheadofprint

Résumé

While neurostimulation technologies are rapidly approaching clinical applications for sensorimotor disorders, the impact of electrical stimulation on network dynamics is still unknown. Given the high degree of shared processing in neural structures, it is critical to understand if neurostimulation affects functions that are related to, but not targeted by, the intervention. Here, we approach this question by studying the effects of electrical stimulation of cutaneous afferents on unrelated processing of proprioceptive inputs. We recorded intraspinal neural activity in four monkeys while generating proprioceptive inputs from the radial nerve. We then applied continuous stimulation to the radial nerve cutaneous branch and quantified the impact of the stimulation on spinal processing of proprioceptive inputs via neural population dynamics. Proprioceptive pulses consistently produce neural trajectories that are disrupted by concurrent cutaneous stimulation. This disruption propagates to the somatosensory cortex, suggesting that electrical stimulation can perturb natural information processing across the neural axis.

Identifiants

pubmed: 38245870
pii: S2211-1247(24)00023-8
doi: 10.1016/j.celrep.2024.113695
pii:
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

113695

Informations de copyright

Copyright © 2024 The Author(s). Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests M.C. and S.R. hold patents in relation to peripheral nerve stimulation. S.R. is the founder of SensArs, a company developing neural interfaces for the peripheral nervous system.

Auteurs

Natalija Katic Secerovic (N)

School of Electrical Engineering, University of Belgrade, 11000 Belgrade, Serbia; The Mihajlo Pupin Institute, University of Belgrade, 11060 Belgrade, Serbia; Laboratory for Neuroengineering, Institute for Robotics and Intelligent Systems, ETH Zürich, 8092 Zürich, Switzerland.

Josep-Maria Balaguer (JM)

Rehab and Neural Engineering Labs, University of Pittsburgh, Pittsburgh, PA 15213, USA; Department of Bioengineering, University of Pittsburgh, Pittsburgh, PA 15213, USA; Center for Neural Basis of Cognition, Pittsburgh, PA, USA.

Oleg Gorskii (O)

Institute of Translational Biomedicine, Saint-Petersburg State University, 199034 Saint-Petersburg, Russia; Pavlov Institute of Physiology, Russian Academy of Sciences, 199034 Saint-Petersburg, Russia; National University of Science and Technology "MISIS," 4 Leninskiy Pr., 119049 Moscow, Russia.

Natalia Pavlova (N)

Institute of Translational Biomedicine, Saint-Petersburg State University, 199034 Saint-Petersburg, Russia.

Lucy Liang (L)

Rehab and Neural Engineering Labs, University of Pittsburgh, Pittsburgh, PA 15213, USA; Department of Bioengineering, University of Pittsburgh, Pittsburgh, PA 15213, USA; Center for Neural Basis of Cognition, Pittsburgh, PA, USA.

Jonathan Ho (J)

Rehab and Neural Engineering Labs, University of Pittsburgh, Pittsburgh, PA 15213, USA; Department of Physical Medicine and Rehabilitation, University of Pittsburgh, Pittsburgh, PA 15213, USA.

Erinn Grigsby (E)

Rehab and Neural Engineering Labs, University of Pittsburgh, Pittsburgh, PA 15213, USA; Department of Physical Medicine and Rehabilitation, University of Pittsburgh, Pittsburgh, PA 15213, USA.

Peter C Gerszten (PC)

Department of Neurological Surgery, University of Pittsburgh, Pittsburgh, PA 15213, USA.

Dzhina Karal-Ogly (D)

National Research Centre "Kurchatov Institute," 123098 Moscow, Russia.

Dmitry Bulgin (D)

National Research Centre "Kurchatov Institute," 123098 Moscow, Russia; Sirius University of Science and Technology, 354340 Sochi, Russia.

Sergei Orlov (S)

National Research Centre "Kurchatov Institute," 123098 Moscow, Russia.

Elvira Pirondini (E)

Rehab and Neural Engineering Labs, University of Pittsburgh, Pittsburgh, PA 15213, USA; Department of Bioengineering, University of Pittsburgh, Pittsburgh, PA 15213, USA; Center for Neural Basis of Cognition, Pittsburgh, PA, USA; Department of Physical Medicine and Rehabilitation, University of Pittsburgh, Pittsburgh, PA 15213, USA; Department of Neurological Surgery, University of Pittsburgh, Pittsburgh, PA 15213, USA; Department of Neurobiology, University of Pittsburgh, Pittsburgh, PA 15213, USA.

Pavel Musienko (P)

Institute of Translational Biomedicine, Saint-Petersburg State University, 199034 Saint-Petersburg, Russia; Sirius University of Science and Technology, 354340 Sochi, Russia; Life Improvement by Future Technologies Center "LIFT," 143025 Moscow, Russia.

Stanisa Raspopovic (S)

Laboratory for Neuroengineering, Institute for Robotics and Intelligent Systems, ETH Zürich, 8092 Zürich, Switzerland. Electronic address: stanisa.raspopovic@hest.ethz.ch.

Marco Capogrosso (M)

Rehab and Neural Engineering Labs, University of Pittsburgh, Pittsburgh, PA 15213, USA; Department of Bioengineering, University of Pittsburgh, Pittsburgh, PA 15213, USA; Center for Neural Basis of Cognition, Pittsburgh, PA, USA; Department of Physical Medicine and Rehabilitation, University of Pittsburgh, Pittsburgh, PA 15213, USA; Department of Neurological Surgery, University of Pittsburgh, Pittsburgh, PA 15213, USA. Electronic address: mcapo@pitt.edu.

Classifications MeSH