Neural Mechanisms Underlying the Establishment of Unimodality in Mouse Primary Visual Cortex

Abstract

Early visual cortex, an area classically defined as a purely unisensory cortex, has been suggested to be influenced by non-visual sensory inputs (Wallace et al., 2004; Iurilli et al., 2011; Vasconcelos et al., 2011; Charbonneau et al., 2012; Liang et al., 2013) and the cross-modal effects are enhanced after blindness (Bavelier, D. & Neville, 2002; Pascual-Leone et al., 2005). Although ectopic or increased neural projections from non-visual sensory areas might be partly responsible for the enhanced cross-modality after blindness in some cases (Karlen et al., 2006), such mechanism cannot explain acute enhancement of cross-modality after short-term blindfolding (Merabet et al., 2007; Merabet et al., 2008). Here I showed that mouse visual cortex was weakly multimodal even at the primary visual cortex (V1) and the cross-modality drastically shifted around the critical period (CP) for visual functions. I found that sound modulations of visual spiking activities are tri-phasic in V1, and the audiovisual interactions followed inverse effectiveness rule as in classically-defined multisensory areas. The inverse effectiveness impaired orientation and direction selectivity of visual response. Furthermore, I showed that auditory influence on V1 was dampened specifically during the CP through balancing of sound-driven excitation and inhibition. Visual experience regulated the cross-modality through GABAergic inhibition, and both soma-targeting and dendrite-targeting interneurons gated the cross-modal inputs in different ways. Finally, I showed that abnormal cross-modality was a common characteristics among three different autistic mouse models, supporting the comorbidity between autism and synesthesia (Baron-Cohen et al., 2013; Neufeld et al., 2013). In particular, autistic BTBR inbred strain exhibited exceptionally large V1 cross-modal auditory response with vision-like properties. My study suggests that the cross-modality regulation during CP is crucial for V1 to functionally mature as ‘visual’ cortex and failure of it might develop synesthesia-like multisensory V1.