Initiating the Development of Multisensory Integration by Manipulating Sensory Experience

TLDR

Superior colliculus neurons develop multisensory integration gradually during early postnatal life, requiring cross‑modal experience; without it they respond to multiple modalities but fail to integrate. The study shows that cross‑modal experience, even when delivered late in life, anesthetized and without learning contingencies, can rapidly trigger multisensory integration in superior colliculus neurons, with repeated exposure to the full stimulus at a location that overlaps the neuron’s receptive fields being essential; once acquired, this integration generalizes to other sites, indicating that the extended developmental window is due to circuitry maturation rather than lack of experience and that integration can occur independently of an alert brain.

Abstract

The multisensory integration capabilities of superior colliculus neurons emerge gradually during early postnatal life as a consequence of experience with cross-modal stimuli. Without such experience neurons become responsive to multiple sensory modalities but are unable to integrate their inputs. The present study demonstrates that neurons retain sensitivity to cross-modal experience well past the normal developmental period for acquiring multisensory integration capabilities. Experience surprisingly late in life was found to rapidly initiate the development of multisensory integration, even more rapidly than expected based on its normal developmental time course. Furthermore, the requisite experience was acquired by the anesthetized brain and in the absence of any of the stimulus–response contingencies generally associated with learning. The key experiential factor was repeated exposure to the relevant stimuli, and this required that the multiple receptive fields of a multisensory neuron encompassed the cross-modal exposure site. Simple exposure to the individual components of a cross-modal stimulus was ineffective in this regard. Furthermore, once a neuron acquired multisensory integration capabilities at the exposure site, it generalized this experience to other locations, albeit with lowered effectiveness. These observations suggest that the prolonged period during which multisensory integration normally appears is due to developmental factors in neural circuitry in addition to those required for incorporating the statistics of cross-modal events; that neurons learn a multisensory principle based on the specifics of experience and can then apply it to other stimulus conditions; and that the incorporation of this multisensory information does not depend on an alert brain.