Effects of Adaptation on Neural Coding by Primary Sensory Interneurons in the Cricket Cercal System

Abstract

Clague, Heather, Frédéric Theunissen, and John P. Miller. Effects of adaptation on neural coding by primary sensory interneurons in the cricket cercal system. J. Neurophysiol. 77: 207–220, 1997. Methods of stochastic systems analysis were applied to examine the effect of adaptation on frequency encoding by two functionally identical primary interneurons of the cricket cercal system. Stimulus reconstructions were obtained from a linear filtering transformation of spike trains elicited in response to bursts of broadband white noise air current stimuli (5–400 Hz). Each linear reconstruction was compared with the actual stimulus in the frequency domain to obtain a measure of waveform coding accuracy as a function of frequency. The term adaptation in this paper refers to the decrease in firing rate of a cell after the onset or increase in power of a white noise stimulus. The increase in firing rate after stimulus offset or decrease in stimulus power is assumed to be a complementary aspect of the same phenomenon. As the spike rate decreased during the course of adaptation, the total amount of information carried about the velocity waveform of the stimulus also decreased. The quality of coding of frequencies between 70 and 400 Hz decreased dramatically. The quality of coding of frequencies between 5 and 70 Hz decreased only slightly or even increased in some cases. The disproportionate loss of information about the higher frequencies could be attributed in part to the more rapid loss of spikes correlated with high-frequency stimulus components than of spikes correlated with low-frequency components. An increase in the responsiveness of a cell to frequencies >70 Hz was correlated with a decrease in the ability of that cell to encode frequencies in the 5–70 Hz range. This nonlinear property could explain the improvement seen in some cases in the coding accuracy of frequencies between 5 and 70 Hz during the course of adaptation. Waveform coding properties also were characterized for fully adapted neurons at several stimulus intensities. The changes in coding observed through the course of adaptiation were similar in nature to those found across stimulus powers. These changes could be accounted for largely by a change in neural sensitivity. The effect of adaptation on the coding of stimulus power was examined by measuring the response curves to steps in stimulus power before and after exposure to an adapting stimulus. Adaptation caused a loss of information about the mean stimulus power but did not cause any improvement in the coding of changes in stimulus power. The unadapted response of the cells did not show any saturation even at the highest powers used in these experiments.