Stimulus dependent transformations between synaptic and spiking receptive fields in auditory cortex

Kyunghee X Kim,Christoph E Schreiner,Craig A Atencio

doi:10.1038/s41467-020-14835-7

Kyunghee X Kim, Christoph E Schreiner + Show 1 more

Open Access

https://doi.org/10.1038/s41467-020-14835-7

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Abstract

Auditory cortex neurons nonlinearly integrate synaptic inputs from the thalamus and cortex, and generate spiking outputs for simple and complex sounds. Directly comparing synaptic and spiking activity can determine whether this input-output transformation is stimulus-dependent. We employ in vivo whole-cell recordings in the mouse primary auditory cortex, using pure tones and broadband dynamic moving ripple stimuli, to examine properties of functional integration in tonal (TRFs) and spectrotemporal (STRFs) receptive fields. Spectral tuning in STRFs derived from synaptic, subthreshold and spiking responses proves to be substantially more selective than for TRFs. We describe diverse spectral and temporal modulation preferences and distinct nonlinearities, and their modifications between the input and output stages of neural processing. These results characterize specific processing differences at the level of synaptic convergence, integration and spike generation resulting in stimulus-dependent transformation patterns in the primary auditory cortex.

Highlights

Auditory cortex neurons nonlinearly integrate synaptic inputs from the thalamus and cortex, and generate spiking outputs for simple and complex sounds
We find that the spectral tuning of spectrotemporal receptive fields (STRFs) in both subthreshold and suprathreshold responses is often much narrower than that of tonal receptive fields (TRFs)
We explored whether the range of spectral integration or frequency selectivity of STRFs differs between neuronal post-synaptic potentials (PSPs) and spikes

Summary

Introduction

Auditory cortex neurons nonlinearly integrate synaptic inputs from the thalamus and cortex, and generate spiking outputs for simple and complex sounds. We describe diverse spectral and temporal modulation preferences and distinct nonlinearities, and their modifications between the input and output stages of neural processing These results characterize specific processing differences at the level of synaptic convergence, integration and spike generation resulting in stimulus-dependent transformation patterns in the primary auditory cortex. Spectral integration and the cellular transformation of information of more complex natural or dynamically modulated artificial sounds should be affected by these nonlinear processes This suggests that receptive fields derived from complex sounds could differ significantly from those derived by combining single pure tone responses. The nonlinearities associated with sub- and suprathreshold STRFs reveal distinct differences This suggests that spectral tuning in the primary auditory cortex (A1) is determined by different underlying influences when processing pure tones and complex stimuli. Examination of synaptic events underlying the generation of post-synaptic potentials (PSPs) reveals clear distinctions in excitatory and inhibitory STRFs further constraining the information transformation in A1

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