Shifts in Coding Properties and Maintenance of Information Transmission during Adaptation in Barrel Cortex

Abstract

Neuronal responses to ongoing stimulation in many systems change over time, or “adapt.” Despite the ubiquity of adaptation, its effects on the stimulus information carried by neurons are often unknown. Here we examine how adaptation affects sensory coding in barrel cortex. We used spike-triggered covariance analysis of single-neuron responses to continuous, rapidly varying vibrissa motion stimuli, recorded in anesthetized rats. Changes in stimulus statistics induced spike rate adaptation over hundreds of milliseconds. Vibrissa motion encoding changed with adaptation as follows. In every neuron that showed rate adaptation, the input–output tuning function scaled with the changes in stimulus distribution, allowing the neurons to maintain the quantity of information conveyed about stimulus features. A single neuron that did not show rate adaptation also lacked input–output rescaling and did not maintain information across changes in stimulus statistics. Therefore, in barrel cortex, rate adaptation occurs on a slow timescale relative to the features driving spikes and is associated with gain rescaling matched to the stimulus distribution. Our results suggest that adaptation enhances tactile representations in primary somatosensory cortex, where they could directly influence perceptual decisions.

Author Summary

Neuronal responses to continued stimulation change over time, or “adapt.” Adaptation can be crucial to our brain's ability to successfully represent the environment: for example, when we move from a dim to a bright scene adaptation adjusts neurons' response to a given light intensity, enabling them to be maximally sensitive to the current range of stimulus variations. We analyzed how adaptation affects sensory coding in the somatosensory “barrel” cortex of the rat, which represents objects touched by the rat's whiskers, or vibrissae. Whiskers endow these nocturnal animals with impressive discrimination abilities: a rat can discern differences in texture as fine as we can distinguish using our fingertips. Neurons in the somatosensory cortex represent whisker vibrations by responding to “kinetic features,” particularly velocity fluctuations. We recorded responses of barrel cortex neurons to carefully controlled whisker motion and slowly varied the overall characteristics of the motion to provide a changing stimulus “context.” We found that stimulus–response relationships change in a particular way: the “tuning functions” that predict a neuron's response to fluctuations in whisker motion rescale according to the current stimulus distribution. The rescaling is just enough to maintain the information conveyed by the response about the stimulus.

Abstract

Cortical neurons adapt their responses to changes in the input statistics of a stimulus, suggesting adaptation enhances stimulus discrimination and perception.