Original ArticlesVisual-auditory interactions modulate saccade-related activity in monkey superior colliculus
Introduction
The intermediate and deep layers of the midbrain superior colliculus (SC) are of crucial importance for the generation of saccadic eye movements [42]. Both electrical stimulation [38] and recording studies [4] have revealed the existence of topographically organized maps of motor space and sensory space. These maps have roughly orthogonal representations of saccade amplitude (or retinal eccentricity) and direction. The rostral half of the primate SC is dedicated to foveal and parafoveal visual space (and saccade amplitudes below 10°). The caudal half of the SC encodes peripheral visual space and is involved in the generation of large-amplitude saccades [34]. Prior to a saccade, a large population of so-called saccade-related burst neurons (SRBNs), located at a specific site within the motor map, is recruited in tight synchrony with the saccade onset 40., 58., and it has been hypothesized that the weighted activity of the entire population determines the amplitude and direction of the saccade vector 20., 22., 34., 49..
A substantial fraction of the SRBNs displays not only motor-related activity, but also produces a sensory evoked burst, that is triggered by the onset of a target in the cell’s receptive field [43]. Although this sensory activity is usually of visual origin, some cells can be activated by auditory or somatosensory stimuli (cat: [25]; monkey: 14., 15.). It has been shown that at the level of single SC cells, the visual, auditory, and somatosensory representations are approximately in register, despite the fundamental differences in initial reference frames (i.e., oculocentric, craniocentric, and body centered, respectively) and encoding formats (retinotopic, tonotopic, and somatotopic, respectively; in cat: 45., 46., 47., 56.; in monkey: [57]).
So far, the neural basis of saccadic eye movements has typically been investigated in orienting tasks involving the rapid foveation of a visual target. Nevertheless, accurate eye movements can be evoked by stimuli of different sensory modalities, and in daily life they are often made in response to peripheral stimuli that emit multimodal sensory cues. Therefore, at the motor programming level, the different sensory modalities need to be merged into a common, oculocentric frame of reference. The neural processing that subserves these multisensory remapping stages is, however, still poorly understood.
Due to both the multisensory convergence onto single cells, and its involvement in the generation of orienting movements of not only the eyes, but also head and ears, the SC is an excellent candidate to study the processes related to multimodal integration. It has been shown in the anesthetized cat that many SC neurons are capable of integrating multimodal stimuli [25]. Often, neurons displayed a strong response enhancement during appropriate bimodal stimulation that well exceeded linear addition of the unimodal responses. In a smaller number of cells, the multimodal interaction resulted in a response suppression [25]. Both multisensory response modes, enhancement, and suppression, have also been reported for SC cells of anesthetized guinea pigs [18] and, more recently, anesthetized monkeys [57].
Because the receptive fields for the various sensory modalities of a multimodally sensitive neuron usually overlap to a considerable degree, the strongest interaction effects were obtained for sensory stimuli presented in both spatial and temporal proximity. Changes in the relative temporal or spatial configurations of auditory and visual stimuli resulted in a systematic decrease of the interaction effect 23., 26., 27., 57..
Multisensory responsive neurons in the SC are thought to play an important role in the programming of goal-directed orienting responses, because the vast majority of these neurons was shown to possess efferent connections to brain stem and spinal motor circuitry 24., 28., 55.. Yet, most experiments on multisensory integration have so far been performed on anesthetized and paralyzed preparations. Due to the absence of orienting movements, research in anesthetized animals is necessarily directed at the sensory activity component of recorded units. Therefore, it is not a priori obvious how to extrapolate these important findings to the fully awake preparation. In particular, conclusions about the relationship between SC motor activity and multisensory-evoked orienting movements of the behaving animal cannot be drawn.
To our knowledge, only a limited amount of multisensory-evoked data is obtained from the behaving animal. A behavioral study with cats [45] has indicated strong effects of auditory-visual integration on the accuracy of visual stimulus localization. Also, a recent study on the human saccadic system reported systematic effects on saccade latency as a function of the visual-auditory stimulus configuration [12]. In addition, the accuracy of eye-head gaze shifts to either visual or auditory targets was shown to be affected by the task requirement, as well as by the temporal and spatial target configuration [3].
Electrophysiological results from the SC of the behaving cat have indicated a visual–auditory interaction effect on the responses of single units [35]. It was reported that some neurons, having saccade-related activity following the onset of a visually evoked eye movement, became presaccadic for saccades toward combined visual–auditory stimuli. Therefore, the timing of the saccade-related burst changed relative to saccade onset as function of the sensory conditions.
Recently, more experimental data on multimodal integration in the SC of the awake cat have become available 29., 36.. In line with earlier findings from anesthetized preparations (described earlier), it was found that a considerable portion of multisensory activated neurons display an enhancement of the sensory-evoked response for bimodal stimuli in the receptive field. The latter group also reported cells that showed a response suppression under these conditions. However, the multisensory effects on movement-related activity were not part of either study. Also, the possible influence of the spatial/temporal stimulus configuration on the multimodal interaction effects were not investigated.
To our knowledge, no data exist on visual–auditory interactions in SRBNs of the SC of the behaving monkey. Therefore, one of the goals of this article is to describe the influence of an auditory stimulus on the response properties of single units in the SC, when the monkey is required to make visually guided saccadic eye movements to various bimodal stimulus configurations.
The present study also addresses recent ideas that assign a prominent role to the collicular output in the precise encoding of the saccade trajectory and kinematics 5., 32., 52., 54.. Note that these theories necessarily predict unique activity patterns for saccades with identical trajectories and kinematics, regardless of the sensory conditions that evoked them. To test this prediction, we have also compared the observed activity changes of combined visual/auditory stimulation to the kinematics and timing of the bimodally evoked saccadic eye movements.
A preliminary account of our findings has been presented in abstract form [9] and in a succinct review [50].
Section snippets
Subjects
Two adult male rhesus monkeys (Macaca mulatta; Sa and Pj) participated in this study. The monkeys were without any apparent visual, auditory, or motor disorder. All experimental procedures were conducted in accordance with national legislation, and with the European Communities Council Directive of November 24, 1986 (86/609/EEC).
Results
Recordings were made from 328 neurons in three colliculi of two monkeys. Of these neurons, 287 displayed clear saccade related activity (Sa: 219; Pj: 68). This fraction of cells was located at deeper sites than the purely visually responsive cells. We collected sufficient data from a total of 50 SRBNs (Sa: 40; Pj: 10) during both the visuomotor and the multisensory task. Of these neurons, 12 also had a clear visual burst (visuo-movement cells), two neurons displayed a transient, very
Discussion
This study provides, for the first time, data on visual–auditory interactions in the SC of the behaving monkey. We believe that the results also have implications for quantitative models on the functional role of the SC in saccade generation. In what follows, these issues will be discussed in more detail.
Conclusion
This article has shown that the motor activity of SRBNs in the monkey SC often depends on the sensory conditions that evoke the saccade. Even though under all conditions the timing of the peak motor activity was tightly linked to saccade onset, the firing rate (as well as the number of spikes) associated with saccades of identical metrics and kinematics could change considerably. Given the large variation in multisensory stimulation patterns that occurs under natural circumstances, it is
Acknowledgements
This work was supported by the University of Nijmegen (AJVO), the Research School Pathophysiology of the Nervous System (MF), and the Mucom II program (6615) of the European ESPRIT initiative. We acknowledge the valuable technical assistance of G. Windau, C. Van der Lee, H. Kleijnen, T. Van Dreumel, and S. Markestijn. Furthermore, we express our gratitude to T. Arts and F. Philipsen from the Central Animal Laboratory, and to Dr. R. Dirksen from the Anesthesiology Department of the University
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