Pure tones modulate the representation of orientation and direction in the primary visual cortex

Abstract

Multimodal sensory integration facilitates the generation of a unified and coherent perception of the environment. It is now well established that unimodal sensory perceptions, such as vision, are improved in multisensory contexts. While multimodal integration is primarily performed by dedicated multisensory brain regions such as the association cortices or the superior colliculus, recent studies have shown that multisensory interactions also occur in primary sensory cortices. In particular, sounds were shown to modulate the responses of neurons located in layers 2/3 (L2/3) of the mouse primary visual cortex (V1). Yet, the net effect of sound modulation at the V1 population level remained unclear. Here, we performed two-photon calcium imaging in awake mice to compare the representation of the orientation and the direction of drifting gratings by V1 L2/3 neurons in unimodal (visual only) or multi-modal (audiovisual) conditions. We found that sound modulation depended on the tuning properties (orientation and direction selectivity) and response amplitudes of V1 L2/3 neurons. Sounds potentiated the responses of neurons that were highly tuned to the cue orientation and direction but weakly active in the unimodal context, following the principle of inverse effectiveness of multimodal integration. Moreover, sound suppressed the responses of neurons untuned for the orientation and/or the direction of the visual cue. Altogether, sound modulation improved the representation of the orientation and direction of the visual stimulus in V1 L2/3. Namely, visual stimuli presented with auditory stimuli recruited a neuronal population better tuned to the visual stimulus orientation and direction than when presented alone.

Complementary Inhibitory Weight Profiles Emerge from Plasticity and Allow Flexible Switching of Receptive Fields

“…SOM + interneurons, on the other hand, could follow a non-Hebbian plasticity rule (e.g., anti-Hebbian or homeostatic), which results in a nonselective connectivity ( Wilson et al, 2012 ). Our second hypothesis posits that changes in the activity of inhibitory neurons are responsible for the highly variable receptive fields observed in recent experiments ( Bathellier et al, 2012 ; Ruff and Cohen, 2014 , 2019 ; Benjamin et al, 2019 ; Billeh et al, 2019 ; McClure and Polack, 2019 ) ( Fig. 1 C ).…”

“…Finally, recent work by Billeh et al (2019) showed that, in mice, visual neurons change their response to the direction of motion of visual stimuli depending on either the temporal or the spatial frequency of the stimulus (drifting grating). These results suggest that receptive fields of sensory neurons are dramatically affected by input (i.e., contextual/attentional states) ( Fritz et al, 2003 ; Kohn and Movshon, 2004 ; Ruff and Cohen, 2014 , 2019 ; Benjamin et al, 2019 ; McClure and Polack, 2019 ), or different aspects of the sensory stimulus ( Bathellier et al, 2012 ; Billeh et al, 2019 ), but it is unclear by which mechanisms such changes can transpire.…”

“…Altered receptive field properties have been widely observed (e.g., in mouse auditory cortex where neurons change their preferred sound frequency with varying sound intensity) ( Bathellier et al, 2012 ). In macaque primary visual cortex (V1), neurons can modulate their response according to an extra cue of a different (auditory) sensory nature ( McClure and Polack, 2019 ). Intriguingly, they responded either more strongly to their preferred stimulus or, on the contrary, they were more suppressed when a pure tone was played alongside the presentation of the visual stimuli.…”

“…B , Initially untuned inhibitory weights (blue lines) acquire different synaptic weight profiles after learning that depend on the excitatory weight profile (red dashed line). C , Contextual changes (e.g., because of attention), which we hypothesize to be responsible for modulating the activity of inhibitory populations, result in different postsynaptic responses to the same stimulus ( Bathellier et al, 2012 ; Ruff and Cohen, 2014 , 2019 ; Benjamin et al, 2019 ; Billeh et al, 2019 ; McClure and Polack, 2019 ), such that preferred (green) and nonpreferred (purple) stimuli elicit postsynaptic responses with different amplitudes.…”

Alignment of Continuous Auditory and Visual Distractor Stimuli Is Leading to an Increased Performance

“…The effect was attributed to an increase in the stochastic resonance. Support for this theory comes from Méndez-Balbuena et al (2015). The authors used a visual pattern reversal task and measured the visual evoked response, while introducing additional tactile noise and found an increase in the P100 amplitude through the noise.…”