ON-OFF receptive fields in auditory cortex diverge during development and contribute to directional sweep selectivity

Joseph Sollini,Paul Chadderton,Gaëlle A. Chapuis,Claudia Clopath

doi:10.1038/s41467-018-04548-3

Joseph Sollini, Paul Chadderton + Show 2 more

Open Access

https://doi.org/10.1038/s41467-018-04548-3

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Abstract

Neurons in the auditory cortex exhibit distinct frequency tuning to the onset and offset of sounds, but the cause and significance of ON and OFF receptive field (RF) organisation are not understood. Here we demonstrate that distinct ON and OFF frequency tuning is largely absent in immature mouse auditory cortex and is thus a consequence of cortical development. Simulations using a novel implementation of a standard Hebbian plasticity model show that the natural alternation of sound onset and offset is sufficient for the formation of non-overlapping adjacent ON and OFF RFs in cortical neurons. Our model predicts that ON/OFF RF arrangement contributes towards direction selectivity to frequency-modulated tone sweeps, which we confirm by neuronal recordings. These data reveal that a simple and universally accepted learning rule can explain the organisation of ON and OFF RFs and direction selectivity in the developing auditory cortex.

Highlights

Neurons in the auditory cortex exhibit distinct frequency tuning to the onset and offset of sounds, but the cause and significance of ON and OFF receptive field (RF) organisation are not understood
We demonstrate that discrete ON/OFF frequency tuning develops following cortical exposure to sound, and complementary Hebbian plasticity of ON and OFF inputs is sufficient for RF reorganisation
Because the selectivity of cortical neurons can be altered by activity-dependent plasticity[18,19,20], we explored whether Hebbian learning underlies the shift in ON/OFF RF arrangement

Summary

Introduction

Neurons in the auditory cortex exhibit distinct frequency tuning to the onset and offset of sounds, but the cause and significance of ON and OFF receptive field (RF) organisation are not understood. In the mature primary auditory cortex (A1), neurons respond to both the onset and offset of sound via activation of non-overlapping populations of synapses[5] These synaptic inputs have discrete frequency tuning, ensuring that individual A1 neurons exhibit distinct frequency selectivity to sound onset and offset[5,6,7,12]. Individual neuron ON and OFF RFs are typically adjacent but non-overlapping with respect to frequency, indicating a high degree of specificity in ON/OFF organisation This specificity may have an anatomical substrate; for instance, ON and OFF inputs could arise from discrete, but adjacent, regions of the auditory thalamus. ON/OFF RF arrangement is related to directional selectivity for slow, ethologically relevant frequency modulations even when synaptic inhibition is reduced, potentially providing a novel mechanism for cortical encoding of vocalisations[17]

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