ATTENTION-LIKE REGULATION OF THETA SWEEPS IN THE BRAIN’S SPATIAL NAVIGATION CIRCUIT

To efficiently navigate in dynamic environments, animals need to focus their spatial attention on selected locations. While the neural underpinnings of spatial attention are unclear, a candidate neural mechanism involves theta-paced sweeps in the population activity of grid and place cells, which sample nearby locations in a left-right-alternating pattern coordinated by upstream parasubicular internal-direction signals. This pattern maximizes uniform coverage of the environment, which may expedite map formation in novel environments, and support updating and retrieval of existing representations in familiar environments. In contrast, in dynamic environments, where animals need to quickly react to changes, a neural correlate of spatial attention would be expected to preferentially cover locations of interest, rather than sweeping rigidly between left and right.
Using large-scale Neuropixels recordings in freely behaving rats, we find that in dynamic environments, sweeps and internal-direction signals rapidly adapt to sample locations of interest: They are spontaneously biased toward fast, erratically moving targets during pursuit and precede orienting responses during immobility. These sweep adaptations can occur without prior spatial learning and during REM sleep. We furthermore show that when the rats’ head- and movement direction differ, such as during backwards walking, sweeps and internal direction extend towards the intended movement direction. Canonical head direction signals from e.g. the anterodorsal thalamus remain locked to true head direction during these adaptations. Collectively, our results frame theta sweeps as a flexible, attention-like mechanism for selectively sampling locations within allocentric cognitive maps.