Coherent encoding of subjective spatial position in visual cortex and hippocampus

Abstract

A major role of vision is to guide navigation, and navigation is strongly driven by vision. Indeed, the brain's visual and navigational systems are known to interact, and signals related to position in the environment have been suggested to appear as early as in the visual cortex. 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.

Neural Correlates of Cognition in Primary Visual versus Neighboring Posterior Cortices during Visual Evidence-Accumulation-based Navigation

“…We discovered the predominant form of neural dynamics in all areas and layers to be the sequential activation of cells. This resembles place cells in the hippocampus (Moser, Kropff, and Moser 2008) , and place preferences have been reported by others in V1 (Saleem et al 2018) . However, most cells were preferentially active on either right-or left-choice trials, a phenomenon previously reported in the PPC (Harvey, Coen, and Tank 2012;Morcos and Harvey 2016) .…”

Sequential and efficient neural-population coding of complex task information

“…Our observations of sequential dynamics in all areas are amongst a growing number of such for the mouse neocortex [53][54][55][56][57][58] . These phenomena are reminiscent of place 76 or time [77][78][79] cells in the hippocampus, which are also known to jointly encode a variety of other spatial and nonspatial factors.…”

Behavior-dependent directional tuning in the human visual-navigation network

“…We believe these two options are not exclusive and the underlying processes might strongly interact in our naturalistic task. Locomotion and world-centered location (Fournier et al, 2019;Saleem et al, 2018) have for example been shown to modulate EVC activity in rodents. Here, we observed that locomotion had a positive effect on model performance in EVC and RSC, suggesting stronger directional tuning in these regions during running (Fig.…”

“…Areas such as the PHG code direction even in the absence of visual experience (Bellmund et al, 2016). In addition, shared information and activity covariations between the EVC and the hippocampal formation suggest that early perceptual processing could well be modulated by higher-level cognitive processes (Bosch et al, 2014;Fournier et al, 2019;Hindy et al, 2016;Kok and Turk-Browne, 2018;Meister and Buffalo, 2016;Nau et al, 2018a;Saleem et al, 2018).…”