Sensory neurons exhibit two universal properties: sensitivity to multiple stimulus dimensions and adaptation to stimulus statistics. How adaptation affects encoding along primary dimensions is well characterized for most sensory pathways, but if and how it affects secondary dimensions is less clear. We studied these effects for neurons in the avian equivalent of primary auditory cortex, responding to temporally-modulated sounds. We showed that the firing rate of single neurons in field L was affected by at least two components of the time-varying sound log-amplitude. When overall sound amplitude was low, neural responses were based on nonlinear combinations of the mean log-amplitude and its rate of change (first time differential). At high mean sound amplitude, the two relevant stimulus features became the first and second time-derivatives of the sound log-amplitude. Thus, a strikingly systematic relationship between dimensions was conserved across changes in stimulus intensity, whereby one of the relevant dimensions approximated the time differential of the other dimension. In contrast to stimulus mean, increases in stimulus variance did not change relevant dimensions, but selectively increased the contribution of the second dimension to neural firing, illustrating a new adaptive behavior enabled by multi-dimensional encoding. Finally, we demonstrated theoretically that inclusion of time differentials as additional stimulus features, as seen so prominently in the single neuron responses studied here, is a useful strategy for encoding naturalistic stimuli, because it can lower the necessary sampling rate while maintaining the robustness of stimulus reconstruction to correlated noise.
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