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Full Access Cross-modal covariance as a key for the maturation of multisensory integration

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Cross-modal covariance as a key for the maturation of multisensory integration

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The ability to integrate information derived from different senses matures over a protracted period of postnatal development. In the superior colliculus (SC), a midbrain structure responsible detecting and orienting to sensory events, this maturational profile is characterized by the gradual appearance of neurons sensitive to more than one modality, and later, by the ability of these neurons to integrate the modality-specific information they receive. It is likely that associative learning principles are at play in guiding multisensory development as the organism gains experience with cross-modal cues. To gain insight into the critical experiential requirements, cats were reared in omnidirectional sound (i.e., noise), a sensory landscape designed to provide co-activation of visual (normal, and discrete) and auditory (ambient, and diffuse) inputs to SC neurons, but to obviate a key requirement of Hebbian-based learning rules via the imposition of uncorrelated noise on one sensory-specific channel (i.e., auditory). The present findings establish that co-activation of sensory-specific SC input channels is not sufficient for SC neurons to develop the ability to integrate cross-modal information. By decoupling cross-modal co-activation and cross-modal co-variance, the noise rearing paradigm provides a key insight lacking from prior studies using dark-rearing or random exposure to visual and auditory stimuli. Thus, the data provide strong evidence that the maturation of SC multisensory integration capabilities requires the encoding of statistical regularities between the cross-modal cues that characterize the rearing environment.

Affiliations: 1: Dept. of Neurobiology & Anatomy, Wake Forest School of Medicine, Winston-Salem, NC, USA

The ability to integrate information derived from different senses matures over a protracted period of postnatal development. In the superior colliculus (SC), a midbrain structure responsible detecting and orienting to sensory events, this maturational profile is characterized by the gradual appearance of neurons sensitive to more than one modality, and later, by the ability of these neurons to integrate the modality-specific information they receive. It is likely that associative learning principles are at play in guiding multisensory development as the organism gains experience with cross-modal cues. To gain insight into the critical experiential requirements, cats were reared in omnidirectional sound (i.e., noise), a sensory landscape designed to provide co-activation of visual (normal, and discrete) and auditory (ambient, and diffuse) inputs to SC neurons, but to obviate a key requirement of Hebbian-based learning rules via the imposition of uncorrelated noise on one sensory-specific channel (i.e., auditory). The present findings establish that co-activation of sensory-specific SC input channels is not sufficient for SC neurons to develop the ability to integrate cross-modal information. By decoupling cross-modal co-activation and cross-modal co-variance, the noise rearing paradigm provides a key insight lacking from prior studies using dark-rearing or random exposure to visual and auditory stimuli. Thus, the data provide strong evidence that the maturation of SC multisensory integration capabilities requires the encoding of statistical regularities between the cross-modal cues that characterize the rearing environment.

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/content/journals/10.1163/22134808-000s0037
2013-05-16
2017-10-17

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