A cerebellar neuroprosthetic system: computational architecture and in vivo test

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• dc.contributor.author Herreros, Ivan
• dc.contributor.author Giovannucci, Andrea
• dc.contributor.author Taub, Aryeh H.
• dc.contributor.author Hogri, Roni
• dc.contributor.author Magal, Ari
• dc.contributor.author Bamford, Sim
• dc.contributor.author Prueckl, Robert
• dc.contributor.author Verschure, Paul F. M. J.
• dc.date.accessioned 2024-01-23T07:16:26Z
• dc.date.available 2024-01-23T07:16:26Z
• dc.date.issued 2014
• dc.description.abstract Emulating the input–output functions performed by a brain structure opens the possibility for developing neuroprosthetic systems that replace damaged neuronal circuits. Here, we demonstrate the feasibility of this approach by replacing the cerebellar circuit responsible for the acquisition and extinction of motor memories. Specifically, we show that a rat can undergo acquisition, retention, and extinction of the eye-blink reflex even though the biological circuit responsible for this task has been chemically inactivated via anesthesia. This is achieved by first developing a computational model of the cerebellar microcircuit involved in the acquisition of conditioned reflexes and training it with synthetic data generated based on physiological recordings. Secondly, the cerebellar model is interfaced with the brain of an anesthetized rat, connecting the model’s inputs and outputs to afferent and efferent cerebellar structures. As a result, we show that the anesthetized rat, equipped with our neuroprosthetic system, can be classically conditioned to the acquisition of an eye-blink response. However, non-stationarities in the recorded biological signals limit the performance of the cerebellar model. Thus, we introduce an updated cerebellar model and validate it with physiological recordings showing that learning becomes stable and reliable. The resulting system represents an important step toward replacing lost functions of the central nervous system via neuroprosthetics, obtained by integrating a synthetic circuit with the afferent and efferent pathways of a damaged brain region. These results also embody an early example of science-based medicine, where on the one hand the neuroprosthetic system directly validates a theory of cerebellar learning that informed the design of the system, and on the other one it takes a step toward the development of neuro-prostheses that could recover lost learning functions in animals and, in the longer term, humans.
• dc.description.sponsorship All the authors were funded by the E.U. project FP7-ICT-2007-1 (ReNaChip 216809). A previous version of this article has been registered as a chapter of Ivan Herreros, Ph.D. thesis. Andrea Giovannucci was supported by a New Jersey Commission on Brain Injury Research fellowship (CBIR12FE1031) and by a Juan de La Cierva contract from the Spanish Ministry of Education. We also acknowledge all partners of the Renachip project contribution to the implementation of this research.
• dc.format.mimetype application/pdf
• dc.identifier.citation Herreros I, Giovannucci A, Taub AH, Hogri R, Magal A, Bamford S, et al. A cerebellar neuroprosthetic system: computational architecture and in vivo test. Front Bioeng Biotechnol. 2014 May 21;2:14. DOI: 10.3389/fbioe.2014.00014
• dc.identifier.doi http://dx.doi.org/10.3389/fbioe.2014.00014
• dc.identifier.issn 2296-4185
• dc.identifier.uri http://hdl.handle.net/10230/58790
• dc.language.iso eng
• dc.publisher Frontiers
• dc.relation.ispartof Frontiers in Bioengineering and Biotechnology. 2014 May 21;2:14
• dc.relation.projectID info:eu-repo/grantAgreement/EC/FP7/216809
• dc.rights © 2014 Herreros, Giovannucci, Taub, Hogri, Magal, Bamford, Prueckl and Verschure. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
• dc.rights.accessRights info:eu-repo/semantics/openAccess
• dc.rights.uri http://creativecommons.org/licenses/by/3.0/
• dc.subject.keyword Neuroprosthetics
• dc.subject.keyword Cerebellum
• dc.subject.keyword Classical conditioning
• dc.subject.keyword Timing
• dc.subject.keyword Memory
• dc.subject.keyword Association learning
• dc.subject.keyword Nucleo-olivary pathway
• dc.subject.keyword Inferior olive
• dc.title A cerebellar neuroprosthetic system: computational architecture and in vivo test
• dc.type info:eu-repo/semantics/article
• dc.type.version info:eu-repo/semantics/publishedVersion