Robust information propagation through noisy neural circuits

PLoS Comput Biol. 2017 Apr 18;13(4):e1005497. doi: 10.1371/journal.pcbi.1005497. eCollection 2017 Apr.

Abstract

Sensory neurons give highly variable responses to stimulation, which can limit the amount of stimulus information available to downstream circuits. Much work has investigated the factors that affect the amount of information encoded in these population responses, leading to insights about the role of covariability among neurons, tuning curve shape, etc. However, the informativeness of neural responses is not the only relevant feature of population codes; of potentially equal importance is how robustly that information propagates to downstream structures. For instance, to quantify the retina's performance, one must consider not only the informativeness of the optic nerve responses, but also the amount of information that survives the spike-generating nonlinearity and noise corruption in the next stage of processing, the lateral geniculate nucleus. Our study identifies the set of covariance structures for the upstream cells that optimize the ability of information to propagate through noisy, nonlinear circuits. Within this optimal family are covariances with "differential correlations", which are known to reduce the information encoded in neural population activities. Thus, covariance structures that maximize information in neural population codes, and those that maximize the ability of this information to propagate, can be very different. Moreover, redundancy is neither necessary nor sufficient to make population codes robust against corruption by noise: redundant codes can be very fragile, and synergistic codes can-in some cases-optimize robustness against noise.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Computational Biology
  • Computer Simulation
  • Models, Neurological*
  • Nerve Net / physiology*
  • Sensory Receptor Cells / physiology*

Grants and funding

JZ’s contribution to this work was partially supported by new faculty start-up funds from the University of Colorado, and by an Azrieli Global Scholar Award from the Canadian Institute For Advanced Research (CIFAR, www.cifar.ca). AP was supported by a grant from the Swiss National Science Foundation, www.snf.ch, (grant #31003A_143707) and by the Simons Collaboration for the Global Brain, www.simonsfoundation.org. PEL was supported by the Gatsby Charitable Foundation, www.gatsby.org.uk. ESB acknowledges the support of National Science Foundation (NSF, www.nsf.gov) Grant CRCNS-1208027 and a Simons Fellowship in Mathematics, and thanks the Allen Institute founders, Paul G. Allen and Jody Allen, for their vision, encouragement and support (www.alleninstitute.org). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.