Initiating the Development of Multisensory Integration by Manipulating Sensory Experience

Liping Yu · Benjamin A. Rowland · Barry E. Stein

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Multisensory perception and integration Visual perception and processing mechanisms Neural dynamics and brain function

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.

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References

1994The merging of the senses 2008Multisensory integration: current issues from the perspective of the single neuron 1986Visual, auditory, and somatosensory convergence on cells in superior colliculus results in multisensory integration 1987Determinants of multisensory integration in superior colliculus neurons. I. Temporal factors 2005Evaluating the Operations Underlying Multisensory Integration in the Cat Superior Colliculus 1997Development of Multisensory Neurons and Multisensory Integration in Cat Superior Colliculus 2009Challenges in quantifying multisensory integration: alternative criteria, models, and inverse effectiveness 2006Early Experience Determines How the Senses Will Interact

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