Optimal behavior relies on the successful integration of complementary information from multiple senses. The neural mechanisms underlying multisensory interactions are still poorly understood. Here, we demonstrate the critical role of neural network oscillations and direct connectivity between primary sensory cortices in visual-somatosensory interactions. Extracellular recordings from all layers of the barrel field in Brown Norway rats in vivo showed that bimodal stimulation (simultaneous light flash and whisker deflection) augmented the somatosensory-evoked response and changed the power of induced network oscillations by resetting their phase. Anatomical tracing revealed sparse direct connectivity between primary visual (V1) and somatosensory (S1) cortices. Pharmacological silencing of V1 diminished but did not abolish cross-modal effects on S1 oscillatory activity, while leaving the early enhancement of the evoked response unaffected. Thus, visual stimuli seem to impact tactile processing by modulating network oscillations in S1 via corticocortical projections and subcortical feedforward interactions.

The hippocampus-driven entrainment of neonatal prefrontal circuits in theta-gamma oscillations contributes to the maturation of cognitive abilities, yet the underlying synaptic mechanisms are still unknown. Here we combine patch-clamp recordings from morphologically and neurochemically characterized layer V pyramidal neurons and interneurons in vivo, with extracellular recordings from the prelimbic cortex (PL) of awake and lightly anesthetized neonatal rats, to elucidate the synaptic framework of early network oscillations. We demonstrate that all neurons spontaneously fire bursts of action potentials. They receive barrages of fast and slow glutamatergic as well as GABAergic synaptic inputs. Oscillatory theta activity results from long-range coupling of pyramidal neurons, presumably within prelimbic-hippocampal circuits, and from local interactions between interneurons. In contrast, beta-low gamma activity requires external glutamatergic drive on prelimbic interneurons. High-frequency oscillations in layer V are independent of interactions at chemical synapses. Thus, specific theta-gamma-modulated synaptic interactions represent the substrate of network oscillations in the developing PL.

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.