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Frequency Adaptation Modulates Spatial Integration of Sensory Responses in the Rat Whisker System

Department of Neuroscience, University of Pennsylvania, Philadelphia, Pennsylvania

Submitted 30 January 2007; accepted in final form 17 March 2007

The generation of perceptual experiences requires the integration of complex spatiotemporal patterns of sensory input. The rodent whisker system is a useful model for understanding the cellular mechanisms of sensory integration, which often include the operation of local circuits distributed throughout the brain. An example is cross-whisker suppression, where the neuronal response to whisker deflection is strongly reduced by preceding deflection of a neighboring whisker. Suppressive interactions between whisker-evoked responses have largely been studied using pairs of single whisker deflections. However, rats typically sweep their whiskers across surfaces at frequencies ranging from 5 to 25 Hz. Repetitive afferent activation induces frequency-dependent adaptation of neuronal responses and alters the synaptic dynamics of circuits that play a role in suppression, suggesting that adaptation could modulate the spatial integration of whisker evoked responses. We tested this hypothesis by comparing the cross-whisker suppression of principal whisker (PW)–evoked cortical and thalamic responses when preceded by either a single deflection of an adjacent whisker (AW) or a train of AW deflections at frequencies covering the normal whisking range. We found that periodic deflection of the preceding AW significantly reduced the magnitude of cross-whisker suppression. Surprisingly, although higher frequencies resulted in greater adaptation of the AW-evoked response, the effect on suppression was independent of frequency. We suggest that these results follow from known local circuit operations at multiple levels within the afferent path. Our findings support the view that repetitive whisking subserves a transformation of the integrative and functional properties of the whisker system.