Error-Robust Modes of the Retinal Population Code
Jason S. Prentice, Olivier Marre, Mark L. Ioffe, Adrianna R. Loback, Gašper Tkačik, Michael J. Berry II
Published: November 17, 2016http://dx.doi.org/10.1371/journal.pcbi.1005148
Across the nervous system, certain population spiking patterns are observed far more frequently than others. A hypothesis about this structure is that these collective activity patterns function as population codewords–collective modes–carrying information distinct from that of any single cell. We investigate this phenomenon in recordings of ∼150 retinal ganglion cells, the retina’s output. We develop a novel statistical model that decomposes the population response into modes; it predicts the distribution of spiking activity in the ganglion cell population with high accuracy. We found that the modes represent localized features of the visual stimulus that are distinct from the features represented by single neurons. Modes form clusters of activity states that are readily discriminated from one another. When we repeated the same visual stimulus, we found that the same mode was robustly elicited. These results suggest that retinal ganglion cells’ collective signaling is endowed with a form of error-correcting code–a principle that may hold in brain areas beyond retina.
Neurons in most parts of the nervous system represent and process information in a collective fashion, yet the nature of this collective code is poorly understood. An important constraint placed on any such collective processing comes from the fact that individual neurons’ signaling is prone to corruption by noise. The information theory and engineering literatures have studied error-correcting codes that allow individual noise-prone coding units to “check” each other, forming an overall representation that is robust to errors. In this paper, we have analyzed the population code of one of the best-studied neural systems, the retina, and found that it is structured in a manner analogous to error-correcting schemes. Indeed, we found that the complex activity patterns over ~150 retinal ganglion cells, the output neurons of the retina, could be mapped onto collective code words, and that these code words represented precise visual information while suppressing noise. In order to analyze this coding scheme, we introduced a novel quantitative model of the retinal output that predicted neural activity patterns more accurately than existing state-of-the-art approaches
Citation: Prentice JS, Marre O, Ioffe ML, Loback AR, Tkačik G, Berry MJ II (2016) Error-Robust Modes of the Retinal Population Code. PLoS Comput Biol 12(11): e1005148. doi:10.1371/journal.pcbi.1005148
Editor: Ian H. Stevenson, University of Connecticut, UNITED STATES
Received: July 15, 2015; Accepted: September 15, 2016; Published: November 17, 2016
Copyright: © 2016 Prentice et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: All supporting data files are available from the Dryad database under doi:10.5061/dryad.1f1rc.
Funding: JSP was supported by a C.V. Starr Fellowship from the Starr Foundation (http://www.starrfoundation.org/). GT was supported by Austrian Research Foundation (https://www.fwf.ac.at/en/) grant FWF P25651. MJB received support from National Eye Institute (https://nei.nih.gov/) grant EY 14196 and from the National Science Foundation grant 1504977. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
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