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Benefits of Pathway Splitting in Sensory Coding

Gjorgjieva, Julijana and Sompolinsky, Haim and Meister, Markus (2014) Benefits of Pathway Splitting in Sensory Coding. Journal of Neuroscience, 34 (36). pp. 12127-12144. ISSN 0270-6474. PMCID PMC4152610. doi:10.1523/JNEUROSCI.1032-14.2014.

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In many sensory systems, the neural signal splits into multiple parallel pathways. For example, in the mammalian retina, ∼20 types of retinal ganglion cells transmit information about the visual scene to the brain. The purpose of this profuse and early pathway splitting remains unknown. We examine a common instance of splitting into ON and OFF neurons excited by increments and decrements of light intensity in the visual scene, respectively. We test the hypothesis that pathway splitting enables more efficient encoding of sensory stimuli. Specifically, we compare a model system with an ON and an OFF neuron to one with two ON neurons. Surprisingly, the optimal ON–OFF system transmits the same information as the optimal ON–ON system, if one constrains the maximal firing rate of the neurons. However, the ON–OFF system uses fewer spikes on average to transmit this information. This superiority of the ON–OFF system is also observed when the two systems are optimized while constraining their mean firing rate. The efficiency gain for the ON–OFF split is comparable with that derived from decorrelation, a well known processing strategy of early sensory systems. The gain can be orders of magnitude larger when the ecologically important stimuli are rare but large events of either polarity. The ON–OFF system also provides a better code for extracting information by a linear downstream decoder. The results suggest that the evolution of ON–OFF diversification in sensory systems may be driven by the benefits of lowering average metabolic cost, especially in a world in which the relevant stimuli are sparse.

Item Type:Article
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URLURL TypeDescription CentralArticle
Gjorgjieva, Julijana0000-0001-7118-4079
Meister, Markus0000-0003-2136-6506
Additional Information:© 2014 the authors. For the first six months after publication SfN’s license will be exclusive. Beginning six months after publication SfN’s license will be non-exclusive and SfN grants the public the non-exclusive right to copy, distribute, or display the Work under a Creative Commons Attribution-NonCommercial-ShareAlike 3.0 Unported license, as described at Received March 14, 2014; revised July 3, 2014; accepted July 22, 2014. This work was supported by a grant from the National Institutes of Health (J.G., H.S. and M.M.) and grants from the Gatsby Charitable Foundation and the Swartz Foundation (H.S.). J.G. thanks Xaq Pitkow for providing help with the sigmoidal nonlinearities from retinal data. Author contributions: J.G., H.S., and M.M. designed research; J.G., H.S., and M.M. performed research; J.G. analyzed data; J.G., H.S., and M.M. wrote the paper. The authors declare no competing financial interests.
Funding AgencyGrant Number
Gatsby Charitable FoundationUNSPECIFIED
Swartz FoundationUNSPECIFIED
Subject Keywords:efficient coding; ON–OFF; optimality; parallel pathways; retina; sensory processing
Issue or Number:36
PubMed Central ID:PMC4152610
Record Number:CaltechAUTHORS:20140911-151331633
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Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:49626
Deposited By: Tony Diaz
Deposited On:11 Sep 2014 23:19
Last Modified:10 Nov 2021 18:46

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