Silencing cortical activity during sound-localization training impairs auditory perceptual learning

Victoria M Bajo,Clio Korn,Edward O Mann,Fernando R Nodal,Andrew J King,Edward S Boyden,Alexandra O Constantinescu

doi:10.1038/s41467-019-10770-4

Abstract

The brain has a remarkable capacity to adapt to changes in sensory inputs and to learn from experience. However, the neural circuits responsible for this flexible processing remain poorly understood. Using optogenetic silencing of ArchT-expressing neurons in adult ferrets, we show that within-trial activity in primary auditory cortex (A1) is required for training-dependent recovery in sound-localization accuracy following monaural deprivation. Because localization accuracy under normal-hearing conditions was unaffected, this highlights a specific role for cortical activity in learning. A1-dependent plasticity appears to leave a memory trace that can be retrieved, facilitating adaptation during a second period of monaural deprivation. However, in ferrets in which learning was initially disrupted by perturbing A1 activity, subsequent optogenetic suppression during training no longer affected localization accuracy when one ear was occluded. After the initial learning phase, the reweighting of spatial cues that primarily underpins this plasticity may therefore occur in A1 target neurons.

Highlights

The brain has a remarkable capacity to adapt to changes in sensory inputs and to learn from experience
To examine the effects of perturbing A1 activity on the performance of the animals in this task, Archaerhodopsin T (ArchT) was expressed in A1 unilaterally by injecting AAV8/CAG-ArchT-green flourescent protein (GFP) or AAV8/CaMKII-ArchTGFP constructs in the dorsal part of the left middle ectosylvian gyrus (Fig. 1b)
ArchT expressing cells were silenced by pairing pulses of green light (λ = 532 nm) generated by a compact diodepumped solid-state (DPSS) laser, delivered via an optical fiber implanted over the location of viral injections in A1, with sound stimulus presentation (Fig. 1a, b, Supplementary Fig. 1)

Summary

Introduction

The brain has a remarkable capacity to adapt to changes in sensory inputs and to learn from experience. Indicating that early auditory cortex is required for adaptation to an imbalance in inputs between the two ears, these approaches lack the temporal specificity necessary to determine at what stage in the learning process A1 is involved or the contribution of different types of cortical neurons. It is not known whether cortical activity following sound presentation during training is sufficient for adaptation to take place or whether A1 is required for learning retrieval when abnormal spatial cues are experienced again. Our findings indicate that retrieval of the adaptive changes induced during learning can occur independently of A1, suggesting that these are likely to be consolidated in neural circuits to which this cortical area projects

Methods

Results

Conclusion