Visual Familiarity Induced 5-Hz Oscillations and Improved Orientation and Direction Selectivities in V1

Neural oscillations play critical roles in information processing, communication between brain areas, learning, and memory. We have recently discovered that familiar visual stimuli can robustly induce 5-Hz oscillations in the primary visual cortex (V1) of awake mice after the visual experience. To gain more mechanistic insight into this phenomenon, we used in vivo patch-clamp recordings to monitor the subthreshold activity of individual neurons during these oscillations. We analyzed the visual tuning properties of V1 neurons in naive and experienced mice to assess the effect of visual experience on the orientation and direction selectivity. Using optogenetic stimulation through the patch pipette in vivo, we measured the synaptic strength of specific intracortical and thalamocortical projections in vivo in the visual cortex before and after the visual experience. We found 5-Hz oscillations in membrane potential (V(m)) and firing rates evoked in single neurons in response to the familiar stimulus, consistent with previous studies. Following the visual experience, the average firing rates of visual responses were reduced while the orientation and direction selectivities were increased. Light-evoked EPSCs were significantly increased for layer 5 (L5) projections to other layers of V1 after the visual experience, while the thalamocortical synaptic strength was decreased. In addition, we developed a computational model that could reproduce 5-Hz oscillations with enhanced neuronal selectivity following synaptic plasticity within the recurrent network and decreased feedforward input. SIGNIFICANCE STATEMENT Neural oscillations at around 5 Hz are involved in visual working memory and temporal expectations in primary visual cortex (V1). However, how the oscillations modulate the visual response properties of neurons in V1 and their underlying mechanism is poorly understood. Here, we show that these oscillations may alter the orientation and direction selectivity of the layer 2/3 (L2/3) neurons and correlate with the synaptic plasticity within V1. Our computational recurrent network model reproduces all these observations and provides a mechanistic framework for studying the role of 5-Hz oscillations in visual familiarity.