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Phase-to-rate transformations encode touch in cortical neurons of a scanning sensorimotor system

Abstract

Sensory perception involves the dual challenge of encoding external stimuli and managing the influence of changes in body position that alter the sensory field. To examine mechanisms used to integrate sensory signals elicited by both external stimuli and motor activity, we recorded from rats trained to rhythmically sweep their vibrissa in search of a target. We found a select population of neurons in primary somatosensory cortex that are transiently excited by the confluence of touch by a single vibrissa and the phase of vibrissa motion in the whisk cycle; different units have different preferred phases. This conditional response enables the rodent to estimate object position in a coordinate frame that is normalized to the trajectory of the motor output, as defined by phase in the whisk cycle, rather than angle of the vibrissa relative to the face. The underlying computation is consistent with gating by an inhibitory shunt.

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Figure 1: Experimental setups and data acquisition.
Figure 2: Free whisking and exemplar touch responses of all single units.
Figure 3: Examples of the interaction between phase in the whisk cycle, as determined from the EMG signal, and the response of rapidly excited touch-sensitive single units.
Figure 4: Summary of the phase sensitivity and spike rate modulation of rapidly excited touch-sensitive single units.
Figure 5: Comparison of the phase dependence versus angular position dependence of the touch response, derived from videographic analysis of vibrissa position, for rapidly excited touch-sensitive single units.
Figure 6: Example of the phase dependence as a function of whisking parameters for a rapidly excited touch-sensitive single unit.
Figure 7: Shunting-inhibition model for the phase sensitivity of active touch.

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Acknowledgements

We thank S.B. Mehta for assistance with spike sorting, E.N. Brown and R.E. Kass for instruction on spike-train analysis, G.A. White for electronics support, E. Ahissar, W. Denk, M. Deschenes, M.E. Diamond, A.L. Fairhall, D.N. Hill and T.J. Sejnowski for relevant discussions, D. Matthews for reading of the manuscript, and the US National Institutes of Health (NS051177), the US National Science Foundation (IGERT) and the US/Israel Binational Foundation (2003222) for financial support.

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Correspondence to David Kleinfeld.

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Curtis, J., Kleinfeld, D. Phase-to-rate transformations encode touch in cortical neurons of a scanning sensorimotor system. Nat Neurosci 12, 492–501 (2009). https://doi.org/10.1038/nn.2283

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