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Development of multisensory integration from the perspective of the individual neuron

Key Points

  • The brain is able to maximize its detection and evaluation of external events by the process of multisensory integration, whereby information from different senses is synthesized and used in concert.

  • Studies of single neurons in animals have revealed that this process is not present at birth, and studies of multisensory neurons in the superior colliculus have provided a developmental model by which the maturation of these neurons can be understood.

  • This integrative capability gradually develops during postnatal life as the underlying neural circuit matures and as the brain acquires experience with cross-modal events.

  • Disruptions of an essential cortical input or the absence of experience with cross-modal events does not preclude the development of multisensory neurons in the superior colliculus. However, it does interfere with the development of a multisensory neuron's capacity to integrate its sensory inputs.

  • Experience also helps to craft the principles by which multisensory integration is instantiated in order to adapt the system to the environment in which it will be used. Thus, abnormal cross-modal experience can alter the principles that normally govern this process.

  • Although multisensory integration capability is most rapidly developed in the young brain, under the proper circumstances even a brain deprived of cross-modal experience early in life can later develop this capability, albeit less efficiently.

Abstract

The ability to use cues from multiple senses in concert is a fundamental aspect of brain function. It maximizes the brain's use of the information available to it at any given moment and enhances the physiological salience of external events. Because each sense conveys a unique perspective of the external world, synthesizing information across senses affords computational benefits that cannot otherwise be achieved. Multisensory integration not only has substantial survival value but can also create unique experiences that emerge when signals from different sensory channels are bound together. However, neurons in a newborn's brain are not capable of multisensory integration, and studies in the midbrain have shown that the development of this process is not predetermined. Rather, its emergence and maturation critically depend on cross-modal experiences that alter the underlying neural circuit in such a way that optimizes multisensory integrative capabilities for the environment in which the animal will function.

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Figure 1: The organization and development of the multisensory superior colliculus.
Figure 2: Developmental profile of multisensory integration in the cat superior colliculus.
Figure 3: A synergy between unisensory subregions of the association cortex drives multisensory integration capabilities in the mature superior colliculus.
Figure 4: The development of multisensory integration depends on concordant experience with cross-modal cues.
Figure 5: Deactivating the association cortex in early life delays the development of multisensory integration.
Figure 6: Adult plasticity in multisensory integration.
Figure 7: Learning to integrate requires a neuron to experience both cues simultaneously.

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Acknowledgements

Portions of the work described here have been supported by US National Institutes of Health grants EY016716 and NS036916 and a grant from the Wallace Foundation.

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Glossary

Multisensory

A process (behaviour) or entity (neuron or circuit) that incorporates information derived from more than one sensory modality.

Multisensory enhancement

The response to a cross-modal stimulus is significantly greater than its responses to either of the component stimuli.

Bayesian frameworks

Statistical frameworks used to model perception in which a feature of the world is inferred based on acquired sensory evidence.

Receptive fields

Regions of external space or location on the body in which stimuli will reliably elicit responses from a given neuron.

Cross-modal stimulus

A stimulus that activates two or more senses.

Spatiotemporal concordance

Closely aligned in space and time.

Spike-timing-dependent plasticity

(STDP). A principle by which synaptic efficacy is strengthened when the presynaptic neuron reliably generates an action potential before the postsynaptic neuron generates an action potential, but is weakened when the reverse relationship occurs or when the activity patterns are decorrelated.

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Stein, B., Stanford, T. & Rowland, B. Development of multisensory integration from the perspective of the individual neuron. Nat Rev Neurosci 15, 520–535 (2014). https://doi.org/10.1038/nrn3742

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