J. William Vaughan

The Development of Cortical Multisensory Integration

Although there are many perceptual theories that posit particular maturational profiles in higher-order (i.e., cortical) multisensory regions, our knowledge of multisensory development is primarily derived from studies of a midbrain structure, the superior colliculus. Therefore, the present study examined the maturation of multisensory processes in an area of cat association cortex [i.e., the anterior ectosylvian sulcus (AES)] and found that these processes are rudimentary during early postnatal life and develop only gradually thereafter. The AES comprises separate visual, auditory, and somatosensory regions, along with many multisensory neurons at the intervening borders between them. During early life, sensory responsiveness in AES appears in an orderly sequence. Somatosensory neurons are present at 4 weeks of age and are followed by auditory and multisensory (somatosensory–auditory) neurons. Visual neurons and visually responsive multisensory neurons are first seen at 12 weeks of age. The earliest multisensory neurons are strikingly immature, lacking the ability to synthesize the cross-modal information they receive. With postnatal development, multisensory integrative capacity matures. The delayed maturation of multisensory neurons and multisensory integration in AES suggests that the higher-order processes dependent on these circuits appear comparatively late in ontogeny.

Cortex Mediates Multisensory But Not Unisensory Integration in Superior Colliculus

Converging cortical influences from the anterior ectosylvian sulcus and the rostral lateral suprasylvian sulcus were shown to have a multisensory-specific role in the integration of sensory information in superior colliculus (SC) neurons. These observations were based on changes induced by cryogenic deactivation of these cortico-SC projections. Thus, although the results indicated that they played a critical role in integrating SC responses to stimuli derived from different senses (i.e., visual–auditory), they played no role in synthesizing its responses to stimuli derived from within the same sense (visual–visual). This was evident even in the same multisensory neurons. The results suggest that very different neural circuits have evolved to code combinations of cross-modal and within-modal stimuli in the SC, and that the differences in multisensory and unisensory integration are likely caused by differences in the configuration of each neurons functional inputs rather than to any inherent differences among the neurons themselves. The specificity of these descending influences was also apparent in the very different ways in which they affected responses to the component cross-modal stimuli and their actual integration. Furthermore, they appeared to target only multisensory neurons and not their unisensory neighbors.

Multisensory integration in the superior colliculus requires synergy among corticocollicular inputs.

Influences from the visual (AEV), auditory (FAES), and somatosensory (SIV) divisions of the cat anterior ectosylvian sulcus (AES) play a critical role in rendering superior colliculus (SC) neurons capable of multisensory integration. However, it is not known whether this is accomplished via their independent sensory-specific action or via some cross-modal cooperative action that emerges as a consequence of their convergence on SC neurons. Using visual–auditory SC neurons as a model, we examined how selective and combined deactivation of FAES and AEV affected SC multisensory (visual–auditory) and unisensory (visual–visual) integration capabilities. As noted earlier, multisensory integration yielded SC responses that were significantly greater than those evoked by the most effective individual component stimulus. This multisensory “response enhancement” was more evident when the component stimuli were weakly effective. Conversely, unisensory integration was dominated by the lack of response enhancement. During cryogenic deactivation of FAES and/or AEV, the unisensory responses of SC neurons were only modestly affected; however, their multisensory response enhancement showed a significant downward shift and was eliminated. The shift was similar in magnitude for deactivation of either AES subregion and, in general, only marginally greater when both were deactivated simultaneously. These data reveal that SC multisensory integration is dependent on the cooperative action of distinct subsets of unisensory corticofugal afferents, afferents whose sensory combination matches the multisensory profile of their midbrain target neurons, and whose functional synergy is specific to rendering SC neurons capable of synthesizing information from those particular senses.