Abstract
Optimal behavior relies on the combination of inputs from multiple senses through complex interactions within neocortical networks. The ontogeny of this multisensory interplay is still unknown. Here, we identify critical factors that control the development of visual-tactile processing by combining in vivo electrophysiology with anatomical/functional assessment of cortico-cortical communication and behavioral investigation of pigmented rats. We demonstrate that the transient reduction of unimodal (tactile) inputs during a short period of neonatal development prior to the first cross-modal experience affects feed-forward subcortico-cortical interactions by attenuating the cross-modal enhancement of evoked responses in the adult primary somatosensory cortex. Moreover, the neonatal manipulation alters cortico-cortical interactions by decreasing the cross-modal synchrony and directionality in line with the sparsification of direct projections between primary somatosensory and visual cortices. At the behavioral level, these functional and structural deficits resulted in lower cross-modal matching abilities. Thus, neonatal unimodal experience during defined developmental stages is necessary for setting up the neuronal networks of multisensory processing.
Highlights
Most environmental events provide inputs to multiple senses that need to be integrated into a unified percept
Focusing on visual-tactile interactions in pigmented rats with good visual acuity, we show that a transient reduction of tactile inputs during neonatal development leads to sparser direct connections between adult primary visual and somatosensory cortices
Anatomical, and behavioral evidence that neonatal unimodal inputs prior to the cross-modal experience are necessary for the correct maturation of multisensory processing by contributing to the setting up of structural and functional coupling within cortical networks
Summary
Most environmental events provide inputs to multiple senses that need to be integrated into a unified percept. Direct cortico-cortical connectivity [8] and feed-forward projections from thalamic nuclei [9] represent possible anatomical substrates of efficient multisensory processing at the cortical level. This multisensory processing in primary sensory areas supports the decoding of behaviorally relevant information and thereby improves task performance [10]. The crucial requirements and processes controlling the development of multisensory interactions at the level of primary sensory cortices remain mechanistically unsolved. This knowledge gap is striking in rodents, which have been shown to express highly multisensory abilities at the level of primary sensory cortices [8]
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