Abstract
It is commonly assumed that neural systems efficiently process natural sensory input. However, the mechanisms by which such efficient processing is achieved, and the consequences for perception and behaviour remain poorly understood. Here we show that small conductance calcium-activated potassium (SK) channels enable efficient neural processing and perception of natural stimuli. Specifically, these channels allow for the high-pass filtering of sensory input, thereby removing temporal correlations or, equivalently, whitening frequency response power. Varying the degree of adaptation through pharmacological manipulation of SK channels reduced efficiency of coding of natural stimuli, which in turn gave rise to predictable changes in behavioural responses that were no longer matched to natural stimulus statistics. Our results thus demonstrate a novel mechanism by which the nervous system can implement efficient processing and perception of natural sensory input that is likely to be shared across systems and species.
Highlights
It is commonly assumed that neural systems efficiently process natural sensory input
We show that SK channels, which are found ubiquitously in the brain[12], mediate efficient processing of natural stimuli by sensory neurons through temporal decorrelation and, importantly, how such processing ensures that perception is matched to natural stimulus statistics at the organismal level
We have shown that electrosensory lateral line lobe (ELL) pyramidal neurons can efficiently process natural stimuli through temporal decorrelation because of fractional differentiation, which ensures that the neural tuning increases as a power law with exponent aneuron that is precisely related to the power law exponent of the stimulus astim
Summary
It is commonly assumed that neural systems efficiently process natural sensory input. Gymnotiform wave-type weakly electric fish sense amplitude modulations (AM) of their self-generated quasi-sinusoidal electric organ discharge (EOD) through peripheral electroreceptors found on their skin These electroreceptors in turn send afferents onto sensory pyramidal neurons within the electrosensory lateral line lobe (ELL) that subsequently project to higher brain areas, thereby mediating perception and behavioural responses[13,14]. Previous studies have shown that peripheral afferents can faithfully encode these both at the single neuron and population levels[31,32,33] Because their tuning was found to be independent of temporal frequency, afferents do not efficiently process natural second-order electrosensory stimulus attributes through temporal whitening[31]. It is not known whether and, if so, how, processing of second-order electrosensory stimulus attributes by these cells is constrained by natural stimulus statistics
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