Developmental dynamics of cross-modality in mouse visual cortex

Maturation of GABAergic circuits in primary visual cortex (V1) opens a critical period (CP), a developmental window of enhanced plasticity for visual functions. However, how inhibition promotes the plasticity remains unclear. Here, we investigated the developmental dynamics of auditory responses and audiovisual interactions in mouse V1. Modulation of V1 spiking activity by a transient sound was temporally dynamic with alternating enhancement and suppression phases. When paired with grating visual stimuli, sound-driven spike enhancement and suppression were weaker and stronger with preferred orientation than with non-preferred orientations, respectively, leading to impaired net orientation selectivity in V1 neurons. Strikingly, the net orientation selectivity was impervious to sound specifically during the CP due to equal total amounts of sound-driven spike enhancements and suppressions. This balance of spike modulations at the CP was achieved by the preferential maturation of sound-driven spike suppression. However, further maturation of sound-driven spike enhancement broke the balance after the CP. Spectral analysis of field potentials revealed the enhancement of a GABA-mediated sound-driven power suppression specifically at CP. Reduction of inhibition by 10-day dark-exposure or genetic deletion of GAD65 gene dampened sound-driven spike suppression in V1. Furthermore, acute suppression of either parvalbumin-expressing (PV) or somatostatinexpressing (SST) neurons suggested their early or late recruitments by sound, respectively. Our results point to the dampened net non-visual sensory influence as one of the functional roles of GABA circuit maturation during a developmental CP. The insensitivity of visual selectivity to sound during the CP may promote functional maturation of V1 as visual cortex.