Audiovisual Modulation in Mouse Primary Visual Cortex Depends on Cross-Modal Stimulus Configuration and Congruency

Abstract

The sensory neocortex is a highly connected associative network that integrates information from multiple senses, even at the level of the primary sensory areas. Although a growing body of empirical evidence supports this view, the neural mechanisms of cross-modal integration in primary sensory areas, such as the primary visual cortex (V1), are still largely unknown. Using two-photon calcium imaging in awake mice, we show that the encoding of audiovisual stimuli in V1 neuronal populations is highly dependent on the features of the stimulus constituents. When the visual and auditory stimulus features were modulated at the same rate (i.e., temporally congruent), neurons responded with either an enhancement or suppression compared with unisensory visual stimuli, and their prevalence was balanced. Temporally incongruent tones or white-noise bursts included in audiovisual stimulus pairs resulted in predominant response suppression across the neuronal population. Visual contrast did not influence multisensory processing when the audiovisual stimulus pairs were congruent; however, when white-noise bursts were used, neurons generally showed response suppression when the visual stimulus contrast was high whereas this effect was absent when the visual contrast was low. Furthermore, a small fraction of V1 neurons, predominantly those located near the lateral border of V1, responded to sound alone. These results show that V1 is involved in the encoding of cross-modal interactions in a more versatile way than previously thought. The neural substrate of cross-modal integration is not limited to specialized cortical association areas but extends to primary sensory areas. Using two-photon imaging of large groups of neurons, we show that multisensory modulation of V1 populations is strongly determined by the individual and shared features of cross-modal stimulus constituents, such as contrast, frequency, congruency, and temporal structure. Congruent audiovisual stimulation resulted in a balanced pattern of response enhancement and suppression compared with unisensory visual stimuli, whereas incongruent or dissimilar stimuli at full contrast gave rise to a population dominated by response-suppressing neurons. Our results indicate that V1 dynamically integrates nonvisual sources of information while still attributing most of its resources to coding visual information.

Auditory motion does not modulate spiking activity in the middle temporal and medial superior temporal visual areas

“…Overall, our results favor the traditional model of cortical multisensory processing, with separate cortical domains for each modality, and multisensory neurons being restricted to intermediate zones between these domains (e.g., Avillac, Ben Hamed, & Duhamel, ; Foxworthy, Clemo, & Meredith, ). Most of the physiological evidence for auditory influences on spiking activity in visual cortex have come from studies in mice (Iurilli et al., ; Meijer et al., ; Olcese et al., ), which have direction connections between the primary visual and primary auditory cortex (Meredith & Lomber, ), reflecting a general scaling rule whereby smaller brains tend to show more direct connectivity across cortical systems (Horvát et al., ; Rosa et al., ). Direct anatomical connections between the visual and auditory cortex in primates have been reported (Cappe & Barone, ; Falchier, Clavagnier, Barone, & Kennedy, ; Palmer & Rosa, , ; Rockland & Ojima, ), but to our knowledge, there is only one study that showed that auditory stimuli can modulate the spiking activity in the visual cortex of primates (Wang et al., ), producing a modest decrease in response latency in awake animals.…”

“…However, studies have now shown that low level sensory cortical areas, historically considered unisensory, can be influenced by other modalities (for a review see Ghazanfar & Schroeder, 2006). In particular, these studies have shown cross-modal influences in the auditory and visual systems (Bizley & King, 2008, 2009Bizley, Nodal, Bajo, Nelken, & King, 2007;Iurilli et al, 2012;Lakatos, Chen, O'Connell, Mills, & Schroeder, 2007;Meijer, Montijn, Pennartz, & Lansink, 2017;Olcese, Iurilli, & Medini, 2013;Schroeder & Foxe, 2002;Wang, Celebrini, Trotter, & Barone, 2008).…”

Sound induces change in orientation preference of V1 neurons: Audio-visual cross-influence

“…Indeed, area A1 sends axons to V1 where they connect to inhibitory interneurons (Iurilli et al, 2012). As summarized by Meijer and authors in their paper (Meijer et al, 2017), auditory stimuli suppress VIP interneurons which inhibit SOM cells which in turn suppresses PV (Parvalbumin; GABAergic interneurons) cells and distal dendrites (involved in non-local synapses) of supragranular pyramidal cells (Gentet, 2012;Meijer et al, 2017). This specific pathway is activated precisely in response only to non-visual inputs (Deneux et al, 2018).…”

Auditory Motion Does Not Modulate Spiking Activity in the Middle Temporal and Medial Superior Temporal Visual Areas

“…Avillac et al, 2007;Foxworthy et al, 2013). Most of the physiological evidence for auditory influences on spiking activity in visual cortex have come from studies in mice (Iurilli et al, 2012;Olcese et al, 2013;Meijer et al, 2017), which have direction connections between the primary visual and primary auditory cortex (Meredith & Lomber, 2017), reflecting a general scaling rule whereby smaller brains tend to show more direct connectivity across cortical systems (Horvát et al, 2016;Rosa et al, 2018). Direct anatomical connections between the visual and auditory cortex in primates have been reported (Falchier et al, 2002;Rockland & Ojima, 2003;Cappe & Barone, 2005;Palmer & Rosa, 2006a, 2006b), but to our knowledge, there is only one study that showed that auditory stimuli can modulate the spiking activity in the visual cortex of primates (Wang et al, 2008), producing a modest decrease in response latency in awake animals.…”

“…However, studies have now shown that low level sensory cortical areas, historically considered unisensory, can be influenced by other modalities (for a review see Ghazanfar and Schroeder, 2006). In particular, these studies have shown cross-modal influences in the auditory and visual systems (Schroeder & Foxe, 2002;Bizley et al, 2007;Lakatos et al, 2007;Bizley & King, 2008, 2009Wang et al, 2008;Iurilli et al, 2012;Olcese et al, 2013;Meijer et al, 2017).…”