Perceived directional heading is represented in the brain by head direction (HD) cells, which fire rapidly when the head is pointed in one direction and become virtually silent when the head is pointed in all other directions. The HD signal is dominantly controlled by the position of visual landmarks, but can be maintained by path integration when familiar landmarks are not available. The neural mechanism(s) that allow path integration to maintain the HD signal have not been investigated, but a possible component of this mechanism is acetylcholine, given that selective cholinergic lesions impair path integration-based navigation. To test this, we recorded HD cell activity from the anterodorsal thalamus while rats foraged for food within a cylinder, or navigated within a dual chamber apparatus, after systemic injection of saline or atropine sulfate. In the cylinder, a prominent cue card served as the sole landmark for a standard session, after which the cue was removed for a no-cue session. Saline or atropine sulfate was then injected, and a second no-cue session was conducted, followed by standard, 90° cue rotation, standard, and no-cue sessions. During the first no-cue session after injection, some cells in atropine-treated rats showed slightly more drift in preferred firing direction (PFD) than control cells, but otherwise appeared to be unaffected by atropine. With the cue rotated 90º, 10 of the 19 (53%) cells in atropine-treated rats and 12 of the 17 (71%) control cells shifted within ± 30° of 90º. In the dual chamber apparatus, rats walked from a familiar cylinder to a novel rectangle via an alleyway, and then returned to the familiar cylinder. Control HD cells (n = 7) showed a slight PFD shift as the rat entered the novel rectangle (mean absolute shift = 17.14 ± 3.80°, range = -30 to 12°), suggesting the HD signal was maintained relatively well between arenas by path integration; upon return, the PFD returned to that of the first session (mean absolute shift = 5.14 ± 1.56°, range = -12 to 6°). In contrast, 7 of the 9 HD cells in atropine-treated rats (78%) showed greater PFD shifts between the familiar cylinder and novel rectangle (mean absolute shift = 86.00 ± 12.17°, angular shift range = -102 to 114°) and between the first and last sessions in the familiar cylinder (mean absolute shift = 24.00 ± 10.16°, angular shift range = 0 to -72°); 2 of the 9 cells (22%) showed considerable PFD drift during the novel rectangle or return cylinder sessions. Thus, acetylcholine is not critical for normal HD cell activity within a familiar environment, but facilitates the stability of the HD signal during both path integration and landmark navigation.
Biological Psychology | Psychology
Ryan M. Yoder, Jeremy H.M. Chan, William N. Butler, and Jeffrey S. Taube (2011).
Acetylcholine Contributes to Head Direction Cell Stability During Path Integration and Landmark Navigation. Presented at Neuroscience 2011, Washington, DC.