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

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.

The precedence effect in spatial hearing emerges only late in the auditory pathway

“…Indeed, despite decades of study, the exact role of AC in spatial hearing remains somewhat unclear, and there may be substantial species differences. Unilateral lesions of AC result in poor performance in localizing brief sound in the contralateral sound field in a variety of species (Cranford et al, 1971;Jenkins, Merzenich, 1984;Kavanagh, Kelly, 1987;Lomber, Malhotra, 2008), while other studies indicate an important role for A1 in recalibrating binaural hearing after periods of partial monaural deprivation (Bajo et al, 2019). However, unilateral lesions on the contralateral AC of rats reportedly did not disrupt the sound localization performance of rats (Kelly, 1980).…”

When and How Does the Auditory Cortex Influence Subcortical Auditory Structures? New Insights About the Roles of Descending Cortical Projections

“…When the animals were trained to re-learn the sound-localization task after unilateral ear occlusion (after plugging one ear), there was a massive drop in performance both in controls and in animals with optogenetic control of A1. Nonetheless, across 10 days of training to perform the task with monaural occlusion (note that plugging one ear change the values of the binaural cues but do not eliminate binaural cues), the control animals considerably improved their performance which was not the case for the animals for which A1 was silenced during each trial during sound delivery ( Figure 4 in Bajo et al, 2019 , Figure 3C ). Thus, suppressing auditory cortex activity did not prevent the animal to normally localized sounds, but impaired the ability to adapt to a unilateral earplug.…”

“…Neural responses driven by broadband stimulation [gray rectangles or combined with laser illumination (green rectangles)]. Modified from Bajo et al (2019) . * P < 0.05, ** P < 0.01.…”

“…Second, silencing auditory cortex neurons (by light stimulation of neurons expressing the proton pump ArchT) during sound presentations in an azimuthal sound-localization task did not impair the initial animals’ behavioral performance ( Bajo et al, 2019 , Figure 3C ): performance of control animals and the animals in which each stimulus presentation was paired with optogenetic silencing of A1 neurons localized broadband noise bursts was equally similar (Figure 1 in Bajo et al, 2019 ). When the animals were trained to re-learn the sound-localization task after unilateral ear occlusion (after plugging one ear), there was a massive drop in performance both in controls and in animals with optogenetic control of A1.…”

Synaptic Mechanisms of Top-Down Control in the Non-Lemniscal Inferior Colliculus

“…Similarly, lesioning visual corticostriatal neurons prevents acquisition, but not performance of a visual detection task (Ruediger and Scanziani, 2020). In the auditory system, chemical lesions of auditory cortico-collicular neurons prevent the experience-dependent recovery of sound localization following monaural hearing loss (Bajo et al, 2010), although auditory cortex becomes dispensable for sound-localization once animals have learned to localize sounds using monaural cues (Bajo et al, 2019). Thus, although necessary for perceptual learning, corticofugal synapses may not be the primary locus of experience-dependent plasticity.…”