Anticipatory head direction signals in anterior thalamus: evidence for a thalamocortical circuit that integrates angular head motion to compute head direction

Abstract

Several regions in the rat brain contain neurons known as head-direction cells, which fire only when the rat's head is facing in a specific direction. Head-direction cells are influenced only by the direction of the head with respect to the static environmental surroundings, and not by the position of the head relative to the body. Each head-direction cell has its own preferred direction of firing, so that together, the population of cells provides a continuous signal of momentary directional heading. Here, head-direction cells were recorded from the post-subicular cortex (PSC) and anterodorsal nucleus (ADN) of the thalamus of freely moving rats. Cell activity was analyzed in relation to both momentary head direction, and the angular velocity of head turns. Head-direction cells in PSC maintained the same directional firing preference, regardless of the angular head velocity. By contrast, head-direction cells in ADN systematically shifted their directional firing preference, as a function of angular head velocity. The ADN cells always shifted their directional tuning peak to the left during clockwise head turns, and to the right during counterclockwise head turns. These results suggest that ADN neurons anticipate the future direction of the head, whereas PSC neurons encode the present direction of the head. Based on these findings, we hypothesize that neurons in PSC and ADN are reciprocally connected to form a thalamocortical circuit, which computes the directional position of the rat's head by integrating the angular motion of the head over time.