Sound-Driven Synaptic Inhibition in Primary Visual Cortex

Abstract

SummaryMultimodal objects and events activate many sensory cortical areas simultaneously. This is possibly reflected in reciprocal modulations of neuronal activity, even at the level of primary cortical areas. However, the synaptic character of these interareal interactions, and their impact on synaptic and behavioral sensory responses are unclear. Here, we found that activation of auditory cortex by a noise burst drove local GABAergic inhibition on supragranular pyramids of the mouse primary visual cortex, via cortico-cortical connections. This inhibition was generated by sound-driven excitation of a limited number of cells in infragranular visual cortical neurons. Consequently, visually driven synaptic and spike responses were reduced upon bimodal stimulation. Also, acoustic stimulation suppressed conditioned behavioral responses to a dim flash, an effect that was prevented by acute blockade of GABAergic transmission in visual cortex. Thus, auditory cortex activation by salient stimuli degrades potentially distracting sensory processing in visual cortex by recruiting local, translaminar, inhibitory circuits.

The multisensory function of the human primary visual cortex

“…In agreement with this notion are data from animals demonstrating auditory as well as somatosensory cross-modal convergence within visual cortex of monkeys Wang et al, 2008), cats (Murata et al, 1965;Spinelli et al, 1968;Morrell, 1972;Majkowski and Sobieszek, 1972;Fishman and Michael, 1973), and mice (Iurilli et al, 2012). For example, Iurilli et al (2012) showed that auditory inputs suppressed visual responses within infragranular layers of primary visual cortex via GABAergic synapses and moreover that this suppression was directly linked to performance (as measured by a conditioned motor response). These authors suggested that auditory inputs degrade the perception of the visual stimulus; something that will need to be reconciled with the many studies showing multisensory and cross-modal enhancement of perception and behaviour (a sampling of which we review here).…”

“…Because source estimations were performed after first Raij et al, 2010), suggesting that pathways for convergence may be the same as those generating interaction effects (although this remains to be more thoroughly examined; reviewed in Meredith et al, 2009 andvan Atteveldt et al, 2014a). In agreement with this notion are data from animals demonstrating auditory as well as somatosensory cross-modal convergence within visual cortex of monkeys Wang et al, 2008), cats (Murata et al, 1965;Spinelli et al, 1968;Morrell, 1972;Majkowski and Sobieszek, 1972;Fishman and Michael, 1973), and mice (Iurilli et al, 2012). For example, Iurilli et al (2012) showed that auditory inputs suppressed visual responses within infragranular layers of primary visual cortex via GABAergic synapses and moreover that this suppression was directly linked to performance (as measured by a conditioned motor response).…”

“…These authors suggested that auditory inputs degrade the perception of the visual stimulus; something that will need to be reconciled with the many studies showing multisensory and cross-modal enhancement of perception and behaviour (a sampling of which we review here). More generally, the work of Iurilli et al (2012) constitutes an important step in not only characterizing the neural bases of multisensory processes across circuit and synaptic levels, but also in linking physiology with behaviour. That said, however, few studies have characterised non-linear neural response interactions in visual cortex of animals; something that will undoubtedly change in the coming years alongside improvements in recording techniques in awake, behaving animals as well as techniques for simultaneous recordings from multiple brain sites (e.g.…”

Homeostatic plasticity and synaptic scaling in the adult mouse auditory cortex

“…7). In other words, synaptic scaling in A1, induced by CHL, restored the cross-modal effects of A1 on V1, which are typically mediated by an intact A1 30,47 . These data suggest that synaptic scaling acts to restore the precise function of neuronal networks without losing information.…”

Distributed neural signatures of natural audiovisual speech and music in the human auditory cortex

“…Accumulating evidence suggests that audiovisual modulations are largely based on modulation of temporal processing, not changes in the overall response amplitudes (Allman et al 2008, Iurilli et al 2012, Lakatos et al 2007. For instance, when monkeys are presented with naturalistic sounds accompanied with matching visual stimulus, firing rate of the neurons in the auditory cortex and inter-trial variability of the activation is decreased (Dahl et al 2010).…”