Abstract
BackgroundVisual, 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 V1. Based on the existence of such AI to V1 projections, we looked for modulation of neuronal visual responses in V1 by an auditory stimulus in the awake behaving monkey.ResultsBehavioral 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 V1 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.ConclusionOur data show that single neurons from a primary sensory cortex such as V1 can integrate sensory information of a different modality, a result that argues against a strict hierarchical model of multisensory integration. Multisensory interaction in V1 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.
Highlights
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
The classical view of multisensory integration, based on anatomical grounds [1], proposes that each sensory modality is processed through separate channels from the sensory receptors to the primary sensory areas and further integrated into associative unimodal areas converging at the level of cognitive polymodal areas [2]
Across the different conditions of stimulation, sRT values were on average 155,0 ms for Mk1 and 167,6 ms for Mk2 which correspond to the range of values reported in other studies using similar experimental conditions)[50]
Summary
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. In primates, neuronal responses to more than one sensory modality have been described in areas higher-up in the hierarchy like the frontal, temporal and parietal lobes [3,4,5,6,7,8,9] While these polysensory areas are the best candidates to support sensory fusion, recent studies in humans have surprisingly revealed that multisensory interactions can take place in early stages of sensory processing, in regions thought to be involved in only one modality [10,11]. It can be inferred that these cortical heteromodal connections, as well as the thalamocortical loop [22,23], could be the anatomical pathway responsible for the visual [24,25,26], somatosensory [27,28] or proprioceptive [29] influences observed in the monkey auditory cortex [30]
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