Sound Improves Neuronal Encoding of Visual Stimuli in Mouse Primary Visual Cortex

• Published in: The Journal of neuroscience 2023-04, Vol.43 (16), p.2885-2906
• Main Authors: Williams, Aaron M, Angeloni, Christopher F, Geffen, Maria N
• Format: Article
• Language: English
• Subjects: Animals; Auditory Cortex - physiology; Auditory tasks; Generalized linear models; Hearing; Information processing; Mice; Movement; Neurons; Neurons - physiology; Photic Stimulation - methods; Primary Visual Cortex; Sensory integration; Sound; Statistical models; Visual cortex; Visual effects; Visual perception; Visual Perception - physiology; Visual stimuli; White noise
• ISSN: 0270-6474; 1529-2401
• DOI: 10.1523/JNEUROSCI.2444-21.2023

In everyday life, we integrate visual and auditory information in routine tasks such as navigation and communication. While concurrent sound can improve visual perception, the neuronal correlates of audiovisual integration are not fully understood. Specifically, it remains unclear whether neuronal firing patters in the primary visual cortex (V1) of awake animals demonstrate similar sound-induced improvement in visual discriminability. Furthermore, presentation of sound is associated with movement in the subjects, but little is understood about whether and how sound-associated movement affects audiovisual integration in V1. Here, we investigated how sound and movement interact to modulate V1 visual responses in awake, head-fixed mice and whether this interaction improves neuronal encoding of the visual stimulus. We presented visual drifting gratings with and without simultaneous auditory white noise to awake mice while recording mouse movement and V1 neuronal activity. Sound modulated activity of 80% of light-responsive neurons, with 95% of neurons increasing activity when the auditory stimulus was present. A generalized linear model (GLM) revealed that sound and movement had distinct and complementary effects of the neuronal visual responses. Furthermore, decoding of the visual stimulus from the neuronal activity was improved with sound, an effect that persisted even when controlling for movement. These results demonstrate that sound and movement modulate visual responses in complementary ways, improving neuronal representation of the visual stimulus. This study clarifies the role of movement as a potential confound in neuronal audiovisual responses and expands our knowledge of how multimodal processing is mediated at a neuronal level in the awake brain. Sound and movement are both known to modulate visual responses in the primary visual cortex; however, sound-induced movement has largely remained unaccounted for as a potential confound in audiovisual studies in awake animals. Here, authors found that sound and movement both modulate visual responses in an important visual brain area, the primary visual cortex, in distinct, yet complementary ways. Furthermore, sound improved encoding of the visual stimulus even when accounting for movement. This study reconciles contrasting theories on the mechanism underlying audiovisual integration and asserts the primary visual cortex as a key brain region participating in tripartite sensory interactions.