Development of the Mechanisms Governing Midbrain Multisensory Integration

The ability to integrate information across multiple senses enhances the brain's ability to detect, localize, and identify external events. This process has been well documented in single neurons in the superior colliculus (SC), which synthesize concordant combinations of visual, auditory, and/or somatosensory signals to enhance the vigor of their responses. This increases the physiological salience of crossmodal events and, in turn, the speed and accuracy of SC-mediated behavioral responses to them. However, this capability is not an innate feature of the circuit and only develops postnatally after the animal acquires sufficient experience with covariant crossmodal events to form links between their modality-specific components. Of critical importance in this process are tectopetal influences from association cortex. Recent findings suggest that, despite its intuitive appeal, a simple generic associative rule cannot explain how this circuit develops its ability to integrate those crossmodal inputs to produce enhanced multisensory responses. The present neurocomputational model explains how this development can be understood as a transition from a default state in which crossmodal SC inputs interact competitively to one in which they interact cooperatively. Crucial to this transition is the operation of a learning rule requiring coactivation among tectopetal afferents for engagement. The model successfully replicates findings of multisensory development in normal cats and cats of either sex reared with special experience. In doing so, it explains how the cortico–SC projections can use crossmodal experience to craft the multisensory integration capabilities of the SC and adapt them to the environment in which they will be used.

SIGNIFICANCE STATEMENT The brain's remarkable ability to integrate information across the senses is not present at birth, but typically develops in early life as experience with crossmodal cues is acquired. Recent empirical findings suggest that the mechanisms supporting this development must be more complex than previously believed. The present work integrates these data with what is already known about the underlying circuit in the midbrain to create and test a mechanistic model of multisensory development. This model represents a novel and comprehensive framework that explains how midbrain circuits acquire multisensory experience and reveals how disruptions in this neurotypic developmental trajectory yield divergent outcomes that will affect the multisensory processing capabilities of the mature brain.