Convergence of inputs from different sensory modalities onto individual neurons is a phenomenon that occurs widely throughout the brain at many phyletic levels and appears to represent a basic neural mechanism by which an organism integrates complex environmental stimuli. In the present study, neurons in the superior colliculus (SC) were used as a model to examine how single neurons deal with simultaneous cues from different sensory modalities (e.g., visual, auditory, somatosensory). The functional result of multisensory convergence on an individual cell was determined by comparing the responses evoked from it by a combined-modality (multimodal) stimulus with those elicited by each (unimodal) component of that stimulus presented alone. Superior colliculus cells exhibited profound changes in their activity when individual sensory stimuli were combined. These "multisensory interactions" were found to be widespread among deep laminae cells and fell into one of two functional categories: response enhancement, characterized by a significant increase in the number of discharges evoked; and response depression, characterized by a significant decrease in the discharges elicited. Multisensory response interactions most often reflected a multiplicative, rather than summative, change in activity. Their absolute magnitude varied from cell to cell and, when stimulus conditions were altered, within the same cell. However, the percentage change of enhanced interactions was generally inversely related to the vigor of the responses that could be evoked by presenting each unimodal stimulus alone and suggest that the potential for response amplification was greatest when responses evoked by individual stimuli were weakest. The majority of cells exhibiting multi-sensory characteristics were demonstrated to have descending efferent projections and thus had access to premotor and motor areas of the brain stem and spinal cord involved in SC-mediated attentive and orientation behaviors. These data show that multisensory convergence provides the descending efferent cells of the SC with a dynamic response character. The responses of these cells and the SC-mediated behaviors that they underlie need not be immutably tied to the presence of any single stimulus, but can vary in response to the particular complex of stimuli present in the environment at any given moment.

One of the most impressive features of the central nervous system is its ability to process information from a variety of stimuli to produce an integrated, comprehensive representation of the external world. In the present study, the temporal disparity among combinations of different sensory stimuli was shown to be a critical factor influencing the integration of multisensory stimuli by superior colliculus neurons. Several temporal principles that govern multisensory integration were revealed: (1) maximal levels of response enhancement were generated by overlapping the peak discharge periods evoked by each modality; (2) the magnitude of this enhancement decayed monotonically to zero as the peak discharge periods became progressively more temporally disparate; (3) with further increases in temporal disparity, the same stimulus combinations that previously produced enhancement could often produce depression; and (4) these kinds of interactions could frequently be predicted from the discharge trains initiated by each stimulus alone. Since multisensory superior colliculus neurons project to premotor areas of the brain stem and spinal cord that control the orientation of the receptor organs (eyes, pinnae, head), they are believed to influence attentive and orientation behaviors. Therefore, it is likely that the temporal relationships of different environmental stimuli that control the activity of these neurons are also a powerful determinant of superior colliculus-mediated attentive and orientation behaviors.

The responses of superior colliculus cells to a given sensory stimulus were influenced by the presence or absence of other sensory cues. By pooling sensory inputs, many superior colliculus cells seem to amplify the effects of subtle environmental cues in certain conditions, whereas in others, responses to normally effective stimuli can be blocked. The observations illustrate the dynamic, interactive nature of the multisensory inputs which characterize the deeper laminae of the superior colliculus.

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Physiological studies have demonstrated that inputs from different sensory modalities converge on, and are integrated by, individual superior colliculus neurons and that this integration is governed by specific spatial rules. The present experiments were an attempt to relate these neural processes to overt behavior by determining if behaviors believed to involve the circuitry of the superior colliculus would show similar multisensory dependencies and be subject to the same rules of integration. The neurophysiological-behavioral parallels proved to be striking. The effectiveness of a stimulus of one modality in eliciting attentive and orientation behaviors was dramatically affected by the presence of a stimulus from another modality in each of the three behavioral paradigms used here. Animals trained to approach a low intensity visual cue had their performance significantly enhanced when a brief, low intensity auditory stimulus was presented at the same location as the visual cue, but their performance was significantly depressed when the auditory stimulus was disparate to it. These effects were independent of the animals' experience with the modifying (i.e. auditory) stimulus and exceeded what might have been predicted statistically based on the animals' performance with each single-modality cue. The multiplicative nature of these multisensory interactions and their dependence on the relative positions and intensities of the two stimuli were all very similar to those observed physiologically for single cells. The few differences that were observed appeared to reflect the fact that understanding integration at the level of the single cell requires reference to the individual cell's multisensory receptive field properties, while at the behavioral level populations of receptive fields must be evaluated. These data illustrate that the rules governing multisensory integration at the level of the single cell also predict responses to these stimuli in the intact behaving organism.