PLoS Computational Biology (Nov 2021)

Nonlinear visuoauditory integration in the mouse superior colliculus

  • Shinya Ito,
  • Yufei Si,
  • Alan M. Litke,
  • David A. Feldheim

Journal volume & issue
Vol. 17, no. 11

Abstract

Read online

Sensory information from different modalities is processed in parallel, and then integrated in associative brain areas to improve object identification and the interpretation of sensory experiences. The Superior Colliculus (SC) is a midbrain structure that plays a critical role in integrating visual, auditory, and somatosensory input to assess saliency and promote action. Although the response properties of the individual SC neurons to visuoauditory stimuli have been characterized, little is known about the spatial and temporal dynamics of the integration at the population level. Here we recorded the response properties of SC neurons to spatially restricted visual and auditory stimuli using large-scale electrophysiology. We then created a general, population-level model that explains the spatial, temporal, and intensity requirements of stimuli needed for sensory integration. We found that the mouse SC contains topographically organized visual and auditory neurons that exhibit nonlinear multisensory integration. We show that nonlinear integration depends on properties of auditory but not visual stimuli. We also find that a heuristically derived nonlinear modulation function reveals conditions required for sensory integration that are consistent with previously proposed models of sensory integration such as spatial matching and the principle of inverse effectiveness. Author summary Integrating visual and auditory stimuli that occur at the same location and time improves our ability to identify and respond to external events. This type of sensory integration is an important brain function, and its deficits are known symptoms of patients with autism and schizophrenia. The Superior Colliculus (SC) is a midbrain structure that plays a critical role in integrating visual and auditory inputs to assess saliency and promote action. Although the response properties of the individual SC neurons to visuoauditory stimuli have been characterized, little is known about the spatial and temporal dynamics of their integration at the population level. Here we recorded the response properties of SC neurons to spatially restricted visual and auditory stimuli using large-scale electrophysiology. We found that the mouse SC contains topographically organized visual and auditory neurons that exhibit nonlinear multisensory integration. We also find that a heuristically derived nonlinear modulation function reveals conditions required for sensory integration that are consistent with previously proposed models of sensory integration. These results open the door to further studies using mice that are designed to determine the circuitry underlying multisensory integration, and the mechanisms used for its development.