Visuo-auditory interactions in the primary visual cortex of the behaving monkey: Electrophysiological evidence

Background: Visual, tactile and auditory information is processed from the periphery to the cortical level through separate channels that target primary sensory cortices, from which it is further distributed to functionally specialized areas. Multisensory integration is classically assigned to higher hierarchical cortical areas, but there is growing electrophysiological evidence in man and monkey of multimodal interactions in areas thought to be unimodal, interactions that can occur at very short latencies. Such fast timing of multisensory interactions rules out the possibility of an origin in the polymodal areas mediated through back projections, but is rather in favor of heteromodal connections such as the direct projections observed in the monkey, from auditory areas (including the primary auditory cortex AI) directly to the primary visual cortex VI. Based on the existence of such AI to VI projections, we looked for modulation of neuronal visual responses in VI by an auditory stimulus in the awake behaving monkey. Results: Behavioral or electrophysiological data were obtained from two behaving monkeys. One monkey was trained to maintain a passive central fixation while a peripheral visual (V) or visuo-auditory (AV) stimulus was presented. From a population of 45 VI neurons, there was no difference in the mean latencies or strength of visual responses when comparing V and AV conditions. In a second active task, the monkey was required to orient his gaze toward the visual or visuo-auditory stimulus. From a population of 49 cells recorded during this saccadic task, we observed a significant reduction in response latencies in the visuo-auditory condition compared to the visual condition (mean 61.0 vs. 64.5 ms) only when the visual stimulus was at midlevel contrast. No effect was observed at high contrast. Conclusion: Our data show that single neurons from a primary sensory cortex such as VI can integrate sensory information of a different modality, a result that argues against a strict hierarchical model of multisensory integration. Multisensory interaction in VI is, in our experiment, expressed by a significant reduction in visual response latencies specifically in suboptimal conditions and depending on the task demand. This suggests that neuronal mechanisms of multisensory integration are specific and adapted to the perceptual features of behavior.