Recurrent network dynamics shape direction selectivity in primary auditory cortex

Destinee A Aponte,Gregory Handy,Brent Doiron,Hiroaki Tsukano,Hiroyuki K Kato,Amber M Kline

doi:10.1038/s41467-020-20590-6

Destinee A Aponte, Gregory Handy + Show 4 more

Open Access

https://doi.org/10.1038/s41467-020-20590-6

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Abstract

Detecting the direction of frequency modulation (FM) is essential for vocal communication in both animals and humans. Direction-selective firing of neurons in the primary auditory cortex (A1) has been classically attributed to temporal offsets between feedforward excitatory and inhibitory inputs. However, it remains unclear how cortical recurrent circuitry contributes to this computation. Here, we used two-photon calcium imaging and whole-cell recordings in awake mice to demonstrate that direction selectivity is not caused by temporal offsets between synaptic currents, but by an asymmetry in total synaptic charge between preferred and non-preferred directions. Inactivation of cortical somatostatin-expressing interneurons (SOM cells) reduced direction selectivity, revealing its cortical contribution. Our theoretical models showed that charge asymmetry arises due to broad spatial topography of SOM cell-mediated inhibition which regulates signal amplification in strongly recurrent circuitry. Together, our findings reveal a major contribution of recurrent network dynamics in shaping cortical tuning to behaviorally relevant complex sounds.

Highlights

Detecting the direction of frequency modulation (FM) is essential for vocal communication in both animals and humans
When direction selectivity index (DSI) was compared against the best frequency (BF) of individual neurons, we found a negative correlation between DSI and BF in both pyramidal (Fig. 1g, h) and GABAergic neurons (Supplementary Fig. 3), with higher absolute DSI values at the edges of A1 tonotopy
Opposite from the temporal offsets hypothesis, the onset timing of IPSCs tended to lead that of EPSCs in the preferred direction (−3.5 ± 2.0 ms, p = 0.100), likely reflecting the slightly broader frequency tuning of IPSCs than EPSCs22,38. These findings argue against temporal offsets between feedforward synaptic inputs as the source of direction selectivity in A1; our results rather indicate that in awake mice, direction selectivity is determined by an asymmetry in total postsynaptic charge between sweep directions

Summary

Introduction

Detecting the direction of frequency modulation (FM) is essential for vocal communication in both animals and humans. One model proposes a delay line mechanism, where stimuli on neighboring parts of a receptive field trigger excitatory inputs with distinct latencies[4], while the second model proposes that non-preferred direction of movement evokes leading inhibition which suppresses spikes triggered by trailing excitation[5] Despite their difference in synaptic mechanisms, these models are similar in that they both attribute direction selectivity to temporal offsets between feedforward synaptic inputs onto an integrating neuron. In contrast to classical models, we found that direction selectivity is not caused by temporal offsets between feedforward synaptic inputs; rather, it is generated due to differential amplification of input signals in the recurrent circuitry between preferred and non-preferred directions These results demonstrate that cortical tuning to temporally complex sensory stimuli are shaped by nonlinear recurrent network dynamics, a conclusion that moves away from the classical idea of feedforward-dominant circuitry

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