Spatial modulation of visual responses arises in cortex with active navigation.

During navigation, the visual responses of neurons in mouse primary visual cortex (V1) are modulated by the animal's spatial position. Here we show that this spatial modulation is similarly present across multiple higher visual areas but negligible in the main thalamic pathway into V1. Similar to hippocampus, spatial modulation in visual cortex strengthens with experience and with active behavior. Active navigation in a familiar environment, therefore, enhances the spatial modulation of visual signals starting in the cortex.

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 ∼20% of V1 neurons were influenced by the physical distance traveled, as were ∼40% of CA1 place cells. Moreover, the firing rate of ∼24% of V1 neurons was modulated by the phase of theta oscillations recorded in CA1 and the response profiles of ∼7% of V1 neurons shifted spatially across the theta cycle, analogous to the phase precession observed in ∼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.

Coherent encoding of subjective spatial position in visual cortex and hippocampus.

A major role of vision is to guide navigation, and navigation is strongly driven by vision1-4. Indeed, the brain's visual and navigational systems are known to interact5,6, and signals related to position in the environment have been suggested to appear as early as in the visual cortex6,7. Here, to establish the nature of these signals, we recorded in the primary visual cortex (V1) and hippocampal area CA1 while mice traversed a corridor in virtual reality. The corridor contained identical visual landmarks in two positions, so that a purely visual neuron would respond similarly at those positions. Most V1 neurons, however, responded solely or more strongly to the landmarks in one position rather than the other. This modulation of visual responses by spatial location was not explained by factors such as running speed. To assess whether the modulation is related to navigational signals and to the animal's subjective estimate of position, we trained the mice to lick for a water reward upon reaching a reward zone in the corridor. Neuronal populations in both CA1 and V1 encoded the animal's position along the corridor, and the errors in their representations were correlated. Moreover, both representations reflected the animal's subjective estimate of position, inferred from the animal's licks, better than its actual position. When animals licked in a given location-whether correctly or incorrectly-neural populations in both V1 and CA1 placed the animal in the reward zone. We conclude that visual responses in V1 are controlled by navigational signals, which are coherent with those encoded in hippocampus and reflect the animal's subjective position. The presence of such navigational signals as early as a primary sensory area suggests that they permeate sensory processing in the cortex.