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Front Neural Circuits. 2016 May 11;10:37. doi: 10.3389/fncir.2016.00037. eCollection 2016.

Push-Pull Receptive Field Organization and Synaptic Depression: Mechanisms for Reliably Encoding Naturalistic Stimuli in V1.

Author information

1
Institut de Neurosciences de la Timone, UMR 7289, Centre National de la Recherche Scientifique - Aix-Marseille UniversitéMarseille, France; Neurobiology and Biophysics, Faculty of Biology, University of FreiburgFreiburg, Germany; Bernstein Center Freiburg, University of FreiburgFreiburg, Germany; Department of Biological Sciences, State University of New York (SUNY-Optometry)New York, NY, USA.
2
Institut de Neurosciences de la Timone, UMR 7289, Centre National de la Recherche Scientifique - Aix-Marseille Université Marseille, France.
3
Unité de Neurosciences, Information et Complexité, UPR Centre National de la Recherche Scientifique 3293 Gif-sur-Yvette, France.
4
Department of Biological Sciences, State University of New York (SUNY-Optometry) New York, NY, USA.
5
Neurobiology and Biophysics, Faculty of Biology, University of FreiburgFreiburg, Germany; Bernstein Center Freiburg, University of FreiburgFreiburg, Germany.

Abstract

Neurons in the primary visual cortex are known for responding vigorously but with high variability to classical stimuli such as drifting bars or gratings. By contrast, natural scenes are encoded more efficiently by sparse and temporal precise spiking responses. We used a conductance-based model of the visual system in higher mammals to investigate how two specific features of the thalamo-cortical pathway, namely push-pull receptive field organization and fast synaptic depression, can contribute to this contextual reshaping of V1 responses. By comparing cortical dynamics evoked respectively by natural vs. artificial stimuli in a comprehensive parametric space analysis, we demonstrate that the reliability and sparseness of the spiking responses during natural vision is not a mere consequence of the increased bandwidth in the sensory input spectrum. Rather, it results from the combined impacts of fast synaptic depression and push-pull inhibition, the later acting for natural scenes as a form of "effective" feed-forward inhibition as demonstrated in other sensory systems. Thus, the combination of feedforward-like inhibition with fast thalamo-cortical synaptic depression by simple cells receiving a direct structured input from thalamus composes a generic computational mechanism for generating a sparse and reliable encoding of natural sensory events.

KEYWORDS:

excitation/inhibition; natural visual stimuli; push-pull receptive field; sensory coding; visual cortex

PMID:
27242445
PMCID:
PMC4862982
DOI:
10.3389/fncir.2016.00037
[Indexed for MEDLINE]
Free PMC Article

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