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Correlated input reveals coexisting coding schemes in a sensory cortex

Nature Neuroscience volume 15, pages 1691–1699 (2012)Cite this article

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Abstract

As in other sensory modalities, one function of the somatosensory system is to detect coherence and contrast in the environment. To investigate the neural bases of these computations, we applied different spatiotemporal patterns of stimuli to rat whiskers while recording multiple neurons in the barrel cortex. Model-based analysis of the responses revealed different coding schemes according to the level of input correlation. With uncorrelated stimuli on 24 whiskers, we identified two distinct functional categories of neurons, analogous in the temporal domain to simple and complex cells of the primary visual cortex. With correlated stimuli, however, a complementary coding scheme emerged: two distinct cell populations, similar to reinforcing and antagonist neurons described in the higher visual area MT, responded specifically to correlations. We suggest that similar context-dependent coexisting coding strategies may be present in other sensory systems to adapt sensory integration to specific stimulus statistics.

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Figure 1: Barrel cortex neurons encode whisker deflections in a common low-dimensional subspace.
Figure 2: STC analysis reveals simple and complex nonlinear functions in response to spatially uncorrelated stimuli.
Figure 3: Neurons' nonlinear functions depend on interwhisker instantaneous correlation.
Figure 4: Center-surround tuning maps of local neurons reveals preference for antagonist center-surround stimulations.
Figure 5: Confirmation of the antagonist tuning of local neurons.
Figure 6: Confirmation of the functional properties of global neurons.
Figure 7: Center and surround phase tuning with temporal delays.

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Acknowledgements

We thank Y. Boubenec for providing the natural whisker stimuli, L. Abbott, L. Bourdieu, A. Davison, V. Ego-Stengel, Y. Frégnac, O. Marre, M. Maravall and H. Sompolinsky for comments on the manuscript, and J. Fournier for advice on the protocol. Funding was provided by ANR (NATACS, HR-CORTEX and TRANSTACT) and the European Community (FET grants FACETS FP6-015879, BrainScaleS FP7-269921 and Brain-i-Nets FP7-243914). S.E.B. was supported by Fondation pour la Recherche Medicale.

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  1. Luc Estebanez and Sami El Boustani: These authors contributed equally to this work.

Authors and Affiliations

  1. Unité de Neurosciences, Information et Complexité, UPR 3293, Centre National de la Recherche Scientifique, Gif sur Yvette, France

    Luc Estebanez, Sami El Boustani, Alain Destexhe & Daniel E Shulz

  2. Institut de Biologie de l'École Normale Supérieure, Institut National de la Santé et de la Recherche Médicale U1024, Centre National de la Recherche Scientifique UMR8197, Paris, France

    Luc Estebanez

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Contributions

L.E. and S.E.B. devised the protocols and analyzed the data with D.E.S. and A.D. L.E. and S.E.B. carried out the extracellular recordings. D.E.S. and A.D. supervised the research. L.E., S.E.B., A.D. and D.E.S. wrote the manuscript.

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Correspondence to Alain Destexhe or Daniel E Shulz.

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Estebanez, L., Boustani, S., Destexhe, A. et al. Correlated input reveals coexisting coding schemes in a sensory cortex. Nat Neurosci 15, 1691–1699 (2012). https://doi.org/10.1038/nn.3258

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