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Sparse temporal coding of elementary tactile features during active whisker sensation

Nature Neuroscience volume 12, pages 792–800 (2009)Cite this article

Abstract

How the brain encodes relevant sensory stimuli in the context of active, natural sensation is not known. During active tactile sensation by rodents, whisker movement across surfaces generates complex whisker micro-motion, including discrete, transient slip-stick events, which carry information about surface properties. We simultaneously measured whisker motion and neural activity in somatosensory cortex (S1) in rats whisking across surfaces. Slip-stick motion events were prominently encoded by one or two low-probability, precisely timed spikes in S1 neurons, resulting in a probabilistically sparse ensemble code. Slips could be efficiently decoded from transient, correlated spiking (∼20-ms time scale) in small (∼100 neuron) populations. Slip responses contributed substantially to increased firing rate and transient firing synchrony on surfaces, and firing synchrony was an important cue for surface texture. Slips are thus a fundamental encoded tactile feature in natural whisker input streams and are represented by sparse, temporally precise, synchronous spiking in S1.

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Figure 1: High-acceleration, high-velocity whisker slips are prominent during active whisking on surfaces.
Figure 2: Recording configuration and single-unit sorting using tetrodes.
Figure 3: Slips drive sparse, precisely timed spikes in S1 neurons.
Figure 4: Slips drive a substantial fraction of spikes during surface whisking.
Figure 5: Slip responses are sparse and probabilistic.
Figure 6: Encoding of slip properties.
Figure 7: Slips are efficiently represented by transient synchronous activity in small neuronal ensembles.
Figure 8: Coding of slips and surfaces by synchronous firing.

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Acknowledgements

We thank P. Martin and S. Pahlavan for assistance with behavioral training, and M. DeWeese, B. Olshausen and Y. Dan for comments on an earlier version of the manuscript. This work was supported by a National Science Foundation Integrative Graduate Education and Traineeship fellowship and a Burroughs Wellcome La Jolla Interfaces in Science fellowship (S.P.J.), by National Science Foundation Faculty Early Career Development Award IOB-0546098, National Science Foundation grant #SBE-0542013 to the Temporal Dynamics of Learning Center and a University of California, San Diego Heiligenberg Professorship (D.E.F.).

Author information

Authors and Affiliations

  1. Computational Neurobiology Graduate Program, University of California, San Diego, La Jolla, California, USA

    Shantanu P Jadhav

  2. Department of Molecular and Cellular Biology and Helen Wills Neuroscience Institute, University of California, Berkeley, Berkeley, California, USA

    Shantanu P Jadhav & Daniel E Feldman

  3. Department of Physics, University of California, San Diego, La Jolla, California, USA

    Jason Wolfe

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  3. Daniel E Feldman
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Contributions

S.P.J., J.W. and D.E.F. designed the experiments. S.P.J. and J.W. performed the experiments. S.P.J. and D.E.F. analyzed the data and wrote the paper. All of the authors discussed the results and commented on the manuscript.

Corresponding author

Correspondence to Daniel E Feldman.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–10 and Supplementary Note (PDF 2421 kb)

Supplementary Video 1

Behavior trial showing whisking on surface. Top view of a rat positioning its nose in the nose poke aperture and whisking on a surface with a single intact whisker (D2) on the right side of the face. Nose poke aperture (bright infrared LED, not visible to the rat), surface position (P150 sandpaper) and whisker imaging plane are labeled. At the end of the trial, rat withdraws to the reward chamber. Video is taken at 119 frames per second (fps), and played back at 10 fps. (MPG 3574 kb)

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Jadhav, S., Wolfe, J. & Feldman, D. Sparse temporal coding of elementary tactile features during active whisker sensation. Nat Neurosci 12, 792–800 (2009). https://doi.org/10.1038/nn.2328

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