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Dynamics of excitation and inhibition underlying stimulus selectivity in rat somatosensory cortex

Nature Neuroscience volume 8, pages 1364–1370 (2005)Cite this article

Abstract

Neurons in sensory systems respond to stimuli within their receptive fields, but the magnitude of the response depends on specific stimulus features. In the rodent whisker system, the response magnitude to the deflection of a particular whisker is, in most cells, dependent on the direction of deflection. Here we use in vivo intracellular recordings from thalamorecipient neurons in layers 3 and 4 of the rat barrel cortex to elucidate the dynamics of the synaptic inputs underlying direction selectivity. We show that cells are direction selective despite a broadly tuned excitatory and inhibitory synaptic input. Selectivity emerges from a direction-dependent temporal shift of excitation relative to inhibition. For preferred direction deflections, excitation precedes inhibition, but as the direction diverges from the preferred, this separation decreases. Our results illustrate a mechanism by which the timing of the synaptic inputs, and not their relative peak amplitudes, primarily determine feature selectivity.

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Figure 1: Direction selectivity in layer 4 barrel neurons.
Figure 2: Excitatory and inhibitory conductances underlying the synaptic responses.
Figure 3: Timing of excitatory and inhibitory conductances as a function of direction.
Figure 4: Dynamics of GE and GI.
Figure 5: Population values.

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Acknowledgements

The authors would like to thank R. Traub for intellectual input throughout the preparation of this manuscript, E. Garcia de Yebenes for her technical assistance and A. Reid and J. Cardin for their useful comments. Sponsored by the Human Frontier Science Program Organization.

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Authors and Affiliations

  1. Department of Neuroscience, University of Pennsylvania School of Medicine, 215 Stemmler Hall, Philadelphia, 19106, Pennsylvania, USA

    W Bryan Wilent & Diego Contreras

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  1. W Bryan Wilent
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Correspondence to Diego Contreras.

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Supplementary information

Supplementary Fig. 1

Gsyn for example cell in Figure 1 recorded under control conditions without QX-314. (PDF 71 kb)

Supplementary Fig. 2

Additional example cell recorded with QX-314 as inFigures 3 and 4. (PDF 312 kb)

Supplementary Fig. 3

Stimulator movements for each direction. (PDF 117 kb)

Supplementary Methods (PDF 24 kb)

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Wilent, W., Contreras, D. Dynamics of excitation and inhibition underlying stimulus selectivity in rat somatosensory cortex. Nat Neurosci 8, 1364–1370 (2005). https://doi.org/10.1038/nn1545

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