Initiating the Development of Multisensory Integration by Manipulating Sensory Experience

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.

Brain circuit–gene expression relationships and neuroplasticity of multisensory cortices in blind children

“…An emerging model suggests that learning is supported through a balance of spine formation and elimination (35). Within the visual system, it has been shown that CREB expression during the development of the superior colliculus correlates with that of the retinocollicular pathway in mice (36) and cats (37). Moreover, CREB changes in V1 occur after visual deprivation in monkeys (38).…”

Development of multisensory integration from the perspective of the individual neuron

“…This occurred even when no overt responses to the stimulus were required and in the absence of any of the reinforcement contingencies that are normally associated with learning. It even occurred when cross-modal experience was provided only when the animal was anaesthetized 79,153,154 . Furthermore, nearly the same proportion of superior colliculus neurons acquired multisensory integration capability in these conditions, and did so with nearly the same enhancement magnitudes, as in normal rearing conditions.…”

Audio-visual localization with hierarchical topographic maps: Modeling the superior colliculus

“…Second, during normal postnatal development, the SC gains the ability to integrate the senses after the first few months. Crucially, however, in abnormal development where one sense is deprived, the ability to learn how to integrate is not lost, and integration is gained after only a short period of exposure to crossmodal stimuli [11]. Here then, the SC not only demonstrates automatic development, detection and alignment of sensory information, but it also shows postdevelopmental adaptation.…”