Adult-onset auditory deprivation enhances attenuation of neural responses in the visual cortex and improves peripheral visual acuity

The ability of the brain to undergo plastic changes throughout the lifespan of an organism is essential to optimize its interactions with its environment. Adaptation to sensory loss is observed as cross-modal recruitment of the cortical areas deprived of their own sensory inputs by the spared senses and as compensatory plasticity of the spared cortical areas. The former is thought to increase the cortical resource for processing information related to the spared modalities and the latter is thought to refine the spared senses. In animal models, synaptic and circuit-level plasticity have been observed in both the deprived primary sensory cortex and in the spared primary sensory cortices. In this study, we examined how the primary visual cortex (V1) adapts to cross-modal auditory deprivation initiated in adult mice of both sexes. To do this, we recorded the stimulus-evoked neural activity in V1 layer 2/3 (L2/3) using 2-photon calcium imaging and presented visual stimuli restricted to either the central or the peripheral visual field. We found that adult-onset deafening intensified the attenuation of stimulus-evoked responses to a range of stimuli, largely in the medial V1 representing the peripheral monocular visual field, without affecting the population decoding capability. Furthermore, adult-onset deaf mice exhibited selective behavioral improvement on peripheral visual acuity for detecting static gratings, without changes in contrast sensitivity for detecting moving gratings. Our findings suggest enhancement of neural attenuation may support compensatory plasticity in adult V1, which may benefit the stimulus encoding efficiency to improve detection of fine peripheral visual features. Significance Statement Losing a sensory modality leads to widespread brain adaptation to enhance the remaining senses. In addition to cross-modal recruitment, which repurposes the deprived brain areas to process the spared senses, there is functional refinement of the spared sensory areas referred to as compensatory plasticity. While plasticity is prominent for early-onset sensory loss, functional compensation is also observed after adult-onset sensory loss. Here, we report that adult-onset deafness in mice accentuates attenuation of visual cortical responses to visual stimuli, especially in the peripheral visual field, with indications of more efficient coding. Additionally, deafened adult mice show rather selective improvement on peripheral visual acuity. Our study suggests a mechanism of compensatory plasticity in the adult visual cortex, which may benefit visual function.