Optimal behavior and survival result from integration of information across sensory systems. Modulation of network activity at the level of primary sensory cortices has been identified as a mechanism of cross-modal integration, yet its cellular substrate is still poorly understood. Here, we uncover the mechanisms by which individual neurons in primary somatosensory (S1) and visual (V1) cortices encode visual-tactile stimuli. For this, simultaneous extracellular recordings were performed from all layers of the S1 barrel field and V1 in Brown Norway rats in vivo and units were clustered and assigned to pyramidal neurons and interneurons. We show that visual-tactile stimulation modulates the firing rate of a relatively low fraction of neurons throughout all cortical layers. Generally, it augments the firing of interneurons and decreases the activity of pyramidal neurons. Moreover, bimodal stimulation shapes the timing of neuronal firing by strengthening the phase-coupling between neuronal discharge and theta-beta band network oscillations as well as by modulating spiking onset. Sparse direct axonal projections between neurons in S1 and V1 seem to time the spike trains between the two cortical areas and thus, may act as a substrate of cross-modal modulation. These results indicate that few cortical neurons mediate multisensory effects in primary sensory areas by directly encoding cross-modal information by their rate and timing of firing.
Significance Statement To optimally interact with the environment, diverse sensory inputs need to be bound together within a unified percept. This process takes place in putatively unisensory neocortical areas. However, the strategies of multisensory coding at the neuronal level remain largely unknown. Here, we show that neurons in primary sensory cortices use a dual code for conveying simultaneous visual and tactile stimuli. First, visual-tactile stimulation affects the firing rates of a small population of pyramidal neurons and interneurons. Second, it enhances the firing precision of individual neurons by augmenting the phase-locking to network oscillations and the coupling strength between spike trains. These data identify rate and temporal coding as neuronal mechanisms of multisensory processing in primary sensory cortices.
Authors report no conflict of interest.
This work was funded by grants from the German Research Foundation (Ha4466/10-1, SPP 1665 (Ha4466/12-1) and SFB 936 (B5) to I.L.H.-O) and the European Research Council (ERC-2015-CoG 681577 to I.L.H.-O.). The authors declare no competing financial interests.