REPRESENTATION AND INTEGRATION OF MULTIPLE SENSORY INPUTS IN PRIMATE SUPERIOR COLLICULUS

1. The properties of visual-, auditory-, and somatosensory-responsive neurons, as well as of neurons responsive to multiple sensory cues (i. e., multisensory), were examined in the superior colliculus of the rhe sus monkey. Although superficial layer neurons responded exclusively t o visual stimuli and visual inputs predominated in deeper layers, ther e was also a rich nonvisual and multisensory representation in the sup erior colliculus. More than a quarter (27.8%) of the deep layer popula tion responded to stimuli from more than a single sensory modality. In contrast, 37% responded only to visual cues, 17.6% to auditory cues, and 17.6% to somatosensory cues. Unimodal- and multisensory-responsive neurons were clustered by modality. Each of these modalities was repr esented in map-like fashion, and the different representations were in alignment with one another. 2. Most deep layer visually responsive ne urons were binocular and exhibited poor selectivity for such stimulus characteristics as orientation, velocity, and direction of movement. S imilarly, most auditory-responsive neurons had contralateral receptive fields and were binaural, but had little frequency selectivity and pr eferred complex, broad-band sounds. Somatosensory-responsive neurons w ere overwhelmingly contralateral, high velocity, and rapidly adapting. Only rarely did somatosensory-responsive neurons require distortion o f subcutaneous tissue for activation. 3. The spatial congruence among the different receptive fields of multisensory neurons was a critical feature underlying their ability to synthesize cross-modal information . 4. Combinations of stimuli could have very different consequences in the same neuron, depending on their temporal and spatial relationship s. Generally, multisensory interactions were evident when pairs of sti muli were separated from one another by <500 ms, and the products of t hese interactions far exceeded the sum of their unimodal components. W hether the combination of stimuli produced response enhancement, respo nse depression, or no interaction depended on the location of the stim uli relative to one another and to their respective receptive fields. Maximal response enhancements were observed when stimuli originated fr om similar locations in space (as when derived from the same event) be cause they fell within the excitatory receptive fields of the same mul tisensory neurons. If, however, the stimuli were spatially disparate s uch that one fell beyond the excitatory borders of its receptive field , either no interaction was produced or this stimulus depressed the ef fectiveness of the other. Furthermore. maximal response interactions w ere seen with the pairing of weakly effective unimodal stimuli. As the individual unimodal stimuli became increasingly effective, the levels of response enhancement to stimulus combinations declined, a principl e referred to as inverse effectiveness. Many of the integrative princi ples seen here in the primate superior colliculus are strikingly simil ar to those observed in the cat. These observations indicate that a se t of common principles of multisensory integration is adaptable in wid ely divergent species living in very different ecological situations. 5. Surprisingly, a few multisensory neurons had individual receptive f ields that were not in register with one another. This has not been no ted in multisensory neurons of other species, and these ''anomalous'' receptive fields could present a daunting problem: stimuli originating from the same general location in space cannot simultaneously fall wi thin their respective receptive fields, a stimulus pairing that may re sult in response depression. Conversely, stimuli that originate from s eparate events and disparate locations (and fall within their receptiv e fields) may result in response enhancement. However, the spatial pri nciple of multisensory integration did not apply in these cases. Stimu li presented within their spatially disparate excitatory receptive fie lds inhibited one another's effectiveness, and spatially coincident st imuli failed to produce an interaction. 6. These observations undersco re the critical nature of developing aligned maps to ensure normal mul tisensory integration and of developing neural and behavioral strategi es to maintain map alignment during overt behaviors.