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Physical principles for scalable neural recoding

Marblestone, Adam H. and Zamft, Bradley M. and Maguire, Yael G. and Shapiro, Mikhail G. and Cybulski, Thaddeus R. and Glaser, Joshua I. and Amodei, Dario and Stranges, P. Benjamin and Kalhor, Reza and Dalrymple, David A. and Seo, Dongjin and Alon, Elad and Maharbiz, Michel M. and Carmena, Jose M. and Rabaey, Jan M. and Boyden, Edward S. and Church, George M. and Kording, Konrad P. (2013) Physical principles for scalable neural recoding. Frontiers in Computational Neuroscience, 7 . Art. No. 137. ISSN 1662-5188. PMCID PMC3807567. https://resolver.caltech.edu/CaltechAUTHORS:20131125-140948447

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Abstract

Simultaneously measuring the activities of all neurons in a mammalian brain at millisecond resolution is a challenge beyond the limits of existing techniques in neuroscience. Entirely new approaches may be required, motivating an analysis of the fundamental physical constraints on the problem. We outline the physical principles governing brain activity mapping using optical, electrical, magnetic resonance, and molecular modalities of neural recording. Focusing on the mouse brain, we analyze the scalability of each method, concentrating on the limitations imposed by spatiotemporal resolution, energy dissipation, and volume displacement. Based on this analysis, all existing approaches require orders of magnitude improvement in key parameters. Electrical recording is limited by the low multiplexing capacity of electrodes and their lack of intrinsic spatial resolution, optical methods are constrained by the scattering of visible light in brain tissue, magnetic resonance is hindered by the diffusion and relaxation timescales of water protons, and the implementation of molecular recording is complicated by the stochastic kinetics of enzymes. Understanding the physical limits of brain activity mapping may provide insight into opportunities for novel solutions. For example, unconventional methods for delivering electrodes may enable unprecedented numbers of recording sites, embedded optical devices could allow optical detectors to be placed within a few scattering lengths of the measured neurons, and new classes of molecularly engineered sensors might obviate cumbersome hardware architectures. We also study the physics of powering and communicating with microscale devices embedded in brain tissue and find that, while radio-frequency electromagnetic data transmission suffers from a severe power–bandwidth tradeoff, communication via infrared light or ultrasound may allow high data rates due to the possibility of spatial multiplexing. The use of embedded local recording and wireless data transmission would only be viable, however, given major improvements to the power efficiency of microelectronic devices.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.3389%2Ffncom.2013.00137DOIArticle
http://www.frontiersin.org/Computational_Neuroscience/10.3389/fncom.2013.00137/abstractPublisherArticle
http://arxiv.org/abs/1306.5709arXivDiscussion Paper
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3807567/PubMed CentralArticle
ORCID:
AuthorORCID
Shapiro, Mikhail G.0000-0002-0291-4215
Additional Information: © 2013 Marblestone, Zamft, Maguire, Shapiro, Cybulski, Glaser, Amodei, Stranges, Kalhor, Dalrymple, Seo, Alon, Maharbiz, Carmena, Rabaey, Boyden, Church and Kording. 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. Received: 07 July 2013; Accepted: 23 September 2013; Published online: 21 October 2013. We thank K. Esvelt for helpful discussionson bioluminescent proteins;D. Boysen for help on the fuel cell calculations; R. Tucker and E. Yablonovitch(http://www.e3s-center.org) for helpful discussions on the energy efficiency of CMOS;C. Xu and C. Schaffer for data on optical attenuation lengths; T. Dean and the participants in his CS379C course at Stanford/Google, including Chris Uhlik and Akram Sadek, for helpful discussions and informative content in the discussion notes (http://www.stanford.edu/class/cs379c/); and L. Wood, R. Koene, S. Rezchikov, A. Bansal, J. Lovelock, A. Payne, R. Barish, N. Donoghue, J. Pillow, W. Shih, P. Yin and J. Hewitt for helpful discussions and feedback on earlier drafts. A. Marblestone is supported by the Fannie and John Hertz Foundation fellowship. D. Dalrymple is supported by the Thiel Foundation. K. Kording is funded in part by the Chicago Biomedical Consortium with support from the Searle Funds at The Chicago Community Trust. E. Boyden is supported by the National Institutes of Health (NIH), the National Science Foundation, the MIT McGovern Institute and Media Lab, the New York Stem Cell Foundation Robertson Investigator Award, the Human Frontiers Science Program, and the Paul Allen Distinguished Investigator in Neuroscience Award. B. Stranges, B. Zamft, R. Kalh or and G. Church acknowledge support from the Office of Naval Research and the NIH Centers of Excellence in Genomic Science. M. Shapiro is supported by the Miller Research Institute, the Burroughs Wellcome Career Award at the Scientific Interface and the W. M. Keck Foundation.
Funders:
Funding AgencyGrant Number
Fannie and John Hertz Foundation FellowshipUNSPECIFIED
Thiel FoundationUNSPECIFIED
Chicago Biomedical ConsortiumUNSPECIFIED
The Chicago Community Trust Searle FundsUNSPECIFIED
NIHUNSPECIFIED
NSFUNSPECIFIED
MIT McGovern InstituteUNSPECIFIED
Media LabUNSPECIFIED
New York Stem Cell Foundation Robertson Investigator AwardUNSPECIFIED
Human Frontiers Science ProgramUNSPECIFIED
Paul Allen Distinguished Investigator in Neuroscience AwardUNSPECIFIED
Office of Naval Research (ONR)UNSPECIFIED
NIH Centers of Excellence in Genomic ScienceUNSPECIFIED
Miller Research InstituteUNSPECIFIED
Burroughs Wellcome Career AwardUNSPECIFIED
W. M. Keck FoundationUNSPECIFIED
Subject Keywords:neural recording; brain activity mapping; electrical recording; optical methods; magnetic resonance imaging; molecular recording; embedded electronics
PubMed Central ID:PMC3807567
Record Number:CaltechAUTHORS:20131125-140948447
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20131125-140948447
Official Citation:Marblestone AH, Zamft BM, Maguire YG, Shapiro MG, Cybulski TR, Glaser JI, Amodei D, Stranges P, Kalhor R, Dalrymple DA, Seo D, Alon E, Maharbiz MM, Carmena JM, Rabaey JM, Boyden ES, Church GM and Kording KP (2013) Physical principles for scalable neural recording. Front. Comput. Neurosci. 7:137. doi: 10.3389/fncom.2013.00137
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:42692
Collection:CaltechAUTHORS
Deposited By: Jason Perez
Deposited On:05 Dec 2013 21:36
Last Modified:03 Oct 2019 06:00

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