Mouse Visual Cortex Is Modulated by Distance Traveled and by Theta Oscillations

The visual responses of neurons in the primary visual cortex (V1) are influenced by the animal's position in the environment [1-5]. V1 responses encode positions that co-fluctuate with those encoded by place cells in hippocampal area CA1 [2, 5]. This correlation might reflect a common influence of non-visual spatial signals on both areas. Place cells in CA1, indeed, do not rely only on vision; their place preference depends on the physical distance traveled [6-11] and on the phase of the 6-9 Hz theta oscillation [12, 13]. Are V1 responses similarly influenced by these non-visual factors? We recorded V1 and CA1 neurons simultaneously while mice performed a spatial task in a virtual corridor by running on a wheel and licking at a reward location. By changing the gain that couples the wheel movement to the virtual environment, we found that similar to 20% of V1 neurons were influenced by the physical distance traveled, as were similar to 40% of CA1 place cells. Moreover, the firing rate of similar to 24% of V1 neurons was modulated by the phase of theta oscillations recorded in CA1 and the response profiles of similar to 7% of V1 neurons shifted spatially across the theta cycle, analogous to the phase precession observed in similar to 37% of CA1 place cells. The influence of theta oscillations on V1 responses was more prominent in putative layer 6. These results reveal that, in a familiar environment, sensory processing in V1 is modulated by the key non-visual signals that influence spatial coding in the hippocampus.