Transient and steady-state dynamics of cortical adaptation

Adaptation is a ubiquitous property of all sensory pathways of the brain and thus likely critical in the encoding of behaviorally relevant sensory information. Despite evidence identifying specific biophysical mechanisms contributing to sensory adaptation, its functional role in sensory encoding is not well understood, particularly in the natural environment where transient rather than steady-state activity could dominate the neuronal representation. Here, we show that the heterogeneous transient and steady-state adaptation dynamics of single cortical neurons in the rat vibrissa system were well characterized by an underlying state variable. The state was directly predictable from temporal response properties that capture the time course of postexcitatory suppression following an isolated vibrissa deflection. Altering the initial state, by preceding the periodic stimulus with an additional vibrissa deflection, strongly influenced single-cell transient cortical adaptation responses. Despite the different transient activity, neurons reached the same steady-state adapted response with a time to steady state that was independent of the initial state. However, the differences in transient activity observed on small time scales were not present when activity was integrated over the longer time scale of a stimulus cycle. Taken together, the results here demonstrate that although adaptation can have significant effects on transient neuronal activity and direction selectivity, a simple measure of the time course of suppression following an isolated stimulus predicted a large portion of the observed adaptation dynamics.