Thalamocortical transmission of visual information in awake mice involves phase synchronization and spike synchrony at high gamma frequencies

Abstract

AbstractSynchronization of neuronal spike activity is thought to play a key role in the transmission of information for sensory processing in the brain, and this synchronization is influenced by oscillatory population activity occurring in multiple frequency ranges at multiple stages of sensory pathways. In the neocortex, gamma frequency oscillations appear to play an important role in synchronizing neuronal ensembles and allowing for selective communication between regions, yet relatively little is known about whether gamma oscillations facilitate transmission of sensory information from thalamus to cortex. Here, we investigate the role of gamma oscillations in promoting synchronous spike activity between the visual thalamus (dLGN) and primary visual cortex (V1) in awake mice, a model sensory system with prominent gamma oscillations that are modulated by visual input. We demonstrate that transmission of visual information to cortex involves phase-synchronized oscillations in the high gamma range (50-90Hz), with concomitant millisecond-scale synchronization of thalamic and cortical spike activity. Transition from a full-field gray image to a high-contrast checkerboard image caused gamma activity to rapidly increase in amplitude, frequency, and bandwidth, yet the gamma oscillations in dLGN and V1 maintained a consistent phase relationship. High contrast stimulation also caused an increase in amplitude of oscillations in the beta and low gamma range, but those were not associated with synchronous thalamic activity. These results indicate a role for high gamma oscillations in mediating the functional connectivity between thalamic and cortical neurons in the visual pathway, a similar role to beta oscillations in primates.\n\nSignificance statementThe mechanisms by which neurons selectively communicate are essential to our understanding of how the brain processes information. Abundant evidence suggests that cortical sensory processing involves the synchronization of high frequency electric field oscillations known as gamma oscillations, which allow groups of neurons to synchronize their spike activity in order to collaboratively process sensory input. Here, we show that oscillations and spikes in the visual thalamocortical pathway of the mouse exhibit synchrony across a broad high gamma frequency range (50-90Hz), suggesting these oscillations play an important role in the relay of visual information to the cortex. This is substantially different from oscillations observed in monkeys, in which gamma is absent in thalamus and beta oscillations support thalamocortical relay.