The Journal of Neurophysiology Vol. 86 No. 2 August 2001, pp. 692-702
Copyright ©2001 by the American Physiological Society

Active Locomotion Increases Peak Firing Rates of Anterodorsal Thalamic Head Direction Cells

Centre National de la Recherche Scientifique-Collège de France, Laboratoire de Physiologie de la Perception et de l'Action, 75231 Paris Cedex 05, France

Zugaro, Michaël B., Eiichi Tabuchi, Céline Fouquier, Alain Berthoz, and Sidney I. Wiener. Active Locomotion Increases Peak Firing Rates of Anterodorsal Thalamic Head Direction Cells. J. Neurophysiol. 86: 692-702, 2001. Head direction (HD) cells discharge selectively in macaques, rats, and mice when they orient their head in a specific ("preferred") direction. Preferred directions are influenced by visual cues as well as idiothetic self-motion cues derived from vestibular, proprioceptive, motor efferent copy, and command signals. To distinguish the relative importance of active locomotor signals, we compared HD cell response properties in 49 anterodorsal thalamic HD cells of six male Long-Evans rats during active displacements in a foraging task as well as during passive rotations. Since thalamic HD cells typically stop firing if the animals are tightly restrained, the rats were trained to remain immobile while drinking water distributed at intervals from a small reservoir at the center of a rotatable platform. The platform was rotated in a clockwise/counterclockwise oscillation to record directional responses in the stationary animals while the surrounding environmental cues remained stable. The peak rate of directional firing decreased by 27% on average during passive rotations (r² = 0.73, P < 0.001). Individual cells recorded in sequential sessions (n = 8) reliably showed comparable reductions in peak firing, but simultaneously recorded cells did not necessarily produce identical responses. All of the HD cells maintained the same preferred directions during passive rotations. These results are consistent with the hypothesis that the level of locomotor activity provides a state-dependent modulation of the response magnitude of AD HD cells. This could result from diffusely projecting neuromodulatory systems associated with motor state.