Origin of visual experience-dependent theta oscillations

Visual experience gives rise to persistent theta oscillations in the mouse primary visual cortex (V1) that are specific to the familiar stimulus. Our recent work demonstrated the presence of these oscillations in higher visual areas (HVAs), where they are synchronized with V1 in a context-dependent manner. However, it remains unclear where these unique oscillatory dynamics originate. To investigate this, we conducted paired extracellular electrophysiological recordings in two visual thalamic nuclei (dorsal lateral geniculate nucleus [dLGN] and lateral posterior nucleus [LP]), the retrosplenial cortex (RSC), and the hippocampus (HPC). Oscillatory activity was not found in either of the thalamic nuclei, but a sparse ensemble of oscillating neurons was observed in both the RSC and HPC, similar to V1. To infer functional connectivity changes between the brain regions, we performed directed information analysis, which indicated a trend toward decreased connectivity in all V1-paired regions, with a consistent increase in V1 → V1 connections, suggesting that the oscillations appear to initiate independently within V1. Lastly, complete NMDA lesioning of the HPC did not abolish theta oscillations in V1 that emerge with familiarity. Altogether, these results suggest that (1) theta oscillations do not originate in the thalamus; (2) RSC exhibits theta oscillations, which may follow V1 given the temporal delay present; and (3) the HPC had a sparse group of neurons, with theta oscillations matching V1; however, lesioning suggests that these oscillations emerge independent of each other. Overall, our findings pave the way for future studies to determine the mechanisms by which diverse inputs and outputs shape this memory-related oscillatory activity in the brain.