Rate and Temporal Coding Convey Multisensory Information in Primary Sensory Cortices

Abstract

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 (PYRs) and interneurons (INs). 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 INs and decreases the activity of PYRs. 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.

A large-scale, standardized physiological survey reveals higher order coding throughout the mouse visual cortex

“…The field has a growing body of evidence showing that the canonical model needs to be enhanced to support more sophisticated visual computation. 5,31 For instance, neurons in mouse V1 show complex visual responses previously associated with higher cortical areas, including pattern selectivity for plaid stimuli 33 Furthermore, the emergence of the rodent as a prominent model of the visual system in recent years has revealed evidence of non-visual computation, including behavioral responses such as reward timing and sequence learning 34 , as well as modulation by multimodal sensory stimuli 35,36 and motor signals. 23,24,37–39…”

Distinct roles of parvalbumin and somatostatin interneurons in the synchronization of spike-times in the neocortex

“…If we had limited our analysis to the synchronization of spike-times irrespective of their iFR, we would not have observed any differences between PV and SST interneurons. This result provides further evidence that, in vivo, spike-timing and firing-rate cannot be considered in isolation [7][8][9] .…”

“…Since spike-time and firing rate co-exist and are not completely dissociable in the spiketiming sequences [7][8][9] , it is important to examine how the synchronization of spike-times depend on the iFR of ISI. Thus, we directly compared the spike-times of synchronized L5 and L6 neurons with that of L4 neurons as a function of the L4 neurons' iFRs.…”

“…Precisely timed spikes that are spatially coordinated or synchronized across multiple neurons with millisecond temporal precision have been shown to encode sensory information about stimuli [1][2][3][4][5][6] . Information is contained in both the spike times 2,5 as well as the instantaneous firing-rate (iFR) of precisely timed spike sequences 1,3 , emphasizing the coexistence of temporal and rate codes during sensory information processing [7][8][9] . Yet, the neural circuit mechanisms supporting the generation of highly synchronized spike sequences across cortical layers remain unknown.…”

“…Theoretical as well as experimental studies have suggested that inhibition can modulate spatial correlation/synchronization of spike-times between nearby neurons [10][11][12] and in neurons across multiple neuronal layers 13,14 . In fact, the latency between excitation and inhibition (E/I latency) has been shown to modulate timing and rate of spike sequences in tandem in vivo [7][8][9] . Thus, E/I latency may have critical role in spatio-temporal synchronization of spike-times.…”