Development Of Multisensory Integration In The Superior Colliculus

Scientists have argued for some time about whether the newborn brain is already capable of engaging in multisensory integration or if it requires postnatal sensory experience to do so. In the perceptual literature this issue has sometimes revolved around a syndrome called synesthesia. The literal meaning of synesthesia is "joining of the senses'' and, in synesthetes, strong modality-specific stimuli initiate not only the "proper" sensations but also sensations that are appropriate for other modalities. For example, a sound is not only heard but also may trigger a specific taste or visual image. These cross-modal effects have recently been related to specific changes in brain activity.

Some investigators hold that synesthesia is the normal condition in neonates—that sensory impressions form a "primitive unity" at birth and that only with age and experience are they differentiated from one another. Others believe quite the opposite—that the senses are differentiated at birth and one must learn to associate among them. Studies of SC neurons in animals seem more consistent with the latter view. In newborn cat there are no multisensory neurons in the SC. Initially, the only sensory-responsive neurons are those that respond to somatosensory cues, presumably to help the neonate in finding the nipple. Auditory responsiveness develops in SC neurons at approximately Postnatal Day 5, and visual responses in the multisensory regions of the structure do not appear until about 3 weeks. Multisensory neurons appear in the second week of life (the first are auditory-somatosensory) and gradually increase in number. Although these neonatal multisensory neurons can respond to cues from different sensory modalities, they cannot integrate them to produce the response enhancement or response depression that is characteristic of the mature SC. In this regard, neonatal multisensory neurons appear very much like the nonintegrative multisensory neurons in adult animals described earlier. It is only after many weeks that adult-like multisensory integration can take place. The initiation of this event in any individual neuron is linked to the maturation of functional inputs to it from association cortex. Thus, early neonatal multisensory neurons, mature nonintegrative neurons, and mature integrative neurons that have been deprived of their inputs from association cortex all respond in the same way to cross-modal cues.

At birth, the rhesus monkey is far more mature than is the cat. It already has a complement of multisensory SC neurons, although one that is not equal to that found in the adult monkey. Nevertheless, like multi-sensory neurons in the neonatal cat, these neurons are incapable of synthesizing cross-modal cues to produce response enhancement. Presumably, these neurons also await the development of cortical influences, but this remains to be determined. Nevertheless, it is safe to say that, based on experiments in cats and monkeys, the newborn SC is incapable of multisensory integration. Whether this is also true of neurons in other polysensory areas of the brain is not known. Most important for perceptual theorists would be testing whether multisensory integration is possible in poly-sensory cortex, and one excellent structure in which to examine this question is association cortex, specifically AES. As noted earlier, AES contains multisensory neurons that form a circuit independent of the SC, and baseline studies of the multisensory properties of adult AES neurons have already been performed.

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