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Neural coding during active somatosensation revealed using illusory touch

Nature Neuroscience volume 16, pages 958–965 (2013)Cite this article

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Abstract

Active sensation requires the convergence of external stimuli with representations of body movements. We used mouse behavior, electrophysiology and optogenetics to dissect the temporal interactions among whisker movement, neural activity and sensation of touch. We photostimulated layer 4 activity in single barrels in a closed loop with whisking. Mimicking touch-related neural activity caused illusory perception of an object at a particular location, but scrambling the timing of the spikes over one whisking cycle (tens of milliseconds) did not abolish the illusion, indicating that knowledge of instantaneous whisker position is unnecessary for discriminating object locations. The illusions were induced only during bouts of directed whisking, when mice expected touch, and in the relevant barrel. Reducing activity biased behavior, consistent with a spike count code for object detection at a particular location. Our results show that mice integrate coding of touch with movement over timescales of a whisking bout to produce perception of active touch.

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Figure 1: Overview of the experimental system and whisking strategy during object location discrimination.
Figure 2: L4 neurons spike with precise latencies during object location discrimination.
Figure 3: Decoding object location and behavioral choice on the basis of L4 spikes.
Figure 4: Optogenetic stimulation mimics touch-evoked spiking in L4 neurons.
Figure 5: Closed-loop photostimulation causes illusory perception of object location.
Figure 6: Precise millisecond-timescale spike latencies are not required for detecting an object at a particular location.
Figure 7: Optogenetic silencing of the C2 column biases behavioral choice toward no responses, which is consistent with spike count coding.
Figure 8: Illusory object location can be evoked only during periods of tactile exploration marked by whisking bouts.

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Acknowledgements

We thank M. Smear, M. Hooks, L. Petreanu, N. Sofroniew, A. Lee, H. Yang, D. Golomb and J. Dudman for comments on the manuscript, N. Sofroniew for valuable suggestions on experiments, S. Michael for histology, S. Sternson and L. Looger (Janelia Farm) for reagents, T. Harris, B. Barbarits, A. Leonardo, C. Culianu, V. Iyer and D. Gutnisky (Janelia Farm) for help with silicon probe recordings and M. Karlsson for help with spike clustering.

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  1. Daniel H O'Connor, Qian-Quan Sun & Daniel Huber

    Present address: Present addresses: The Solomon H. Snyder Department of Neuroscience and Brain Science Institute, Johns Hopkins University School of Medicine, Baltimore, Maryland, USA (D.H.O.), Department of Zoology and Physiology, University of Wyoming, Laramie, Wyoming, USA (Q.-Q.S.) and Department of Basic Neurosciences, University of Geneva, Geneva, Switzerland (D.H.).,

  2. Daniel H O'Connor and S Andrew Hires: These authors contributed equally to this work.

Authors and Affiliations

  1. Janelia Farm Research Campus, Howard Hughes Medical Institute, Ashburn, Virginia, USA

    Daniel H O'Connor, S Andrew Hires, Zengcai V Guo, Nuo Li, Jianing Yu, Qian-Quan Sun, Daniel Huber & Karel Svoboda

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Contributions

D.H.O., S.A.H., Z.V.G., N.L., J.Y. and Q.-Q.S. performed experiments. D.H., Z.V.G. and N.L. developed the symmetric response task paradigm. D.H.O., S.A.H. and K.S. planned the project. D.H.O., S.A.H., Z.V.G., N.L. and K.S. analyzed the data. D.H.O., S.A.H. and K.S. wrote the paper with comments from the other authors.

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Correspondence to Karel Svoboda.

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O'Connor, D., Hires, S., Guo, Z. et al. Neural coding during active somatosensation revealed using illusory touch. Nat Neurosci 16, 958–965 (2013). https://doi.org/10.1038/nn.3419

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