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Journal of Neuroscience, Vol 15, 70-86, Copyright © 1995 by Society for Neuroscience
Head direction cells recorded in the anterior thalamic nuclei of freely moving rats
JS Taube
Department of Psychology, Dartmouth College, Hanover, New Hampshire 03755.
Previous studies have identified neurons in the postsubiculum which
discharge as a function of the animal's head direction in the horizontal
plane, independent of its behavior and location in the environment.
Anatomical studies have shown that the postsubiculum contains reciprocal
connections with the anterior thalamic nuclei (ATN). In order to determine
how the head direction (HD) cell signal is processed in the brain,
single-unit recordings were monitored in the ATN of freely moving rats in
order to characterize their behavioral and spatial correlates. Animals were
trained to retrieve food pellets thrown randomly into a cylindrical
apparatus containing a single orientation cue. Single unit recordings in
the ATN showed that approximately 60% of the recorded cells discharged in
relation to the animal's head direction in the horizontal plane.
Observation of the animal and quantitative analyses showed that HD cell
firing was not dependent on the animal's behavior, trunk position, linear
speed, angular head velocity, or location in the environment. Most of these
cells were localized to the anterior dorsal thalamic nucleus. Each HD cell
contained only one head direction at which the cell discharged maximally
and the firing rate decreased linearly away from this preferred direction.
The preferred firing directions from all cells recorded were distributed
over a 360 degrees range. Quantitative analysis showed that these cells
contained similar discharge parameters (peak firing rate, directional
firing range) to values reported previously for postsubicular HD cells
(Taube et al., 1990a). Experiments involving rotation of the orientation
cue showed that the preferred firing direction could be controlled by a
salient visual cue. In contrast to postsubicular HD cells, passive rotation
of a restrained animal showed that most ATN HD cells ceased discharging
when the animal's head was oriented in the preferred direction. These
findings demonstrate the presence of HD cells in the ATN and indicate the
potential importance of this area for spatial navigation. The origin of the
head direction signal is discussed and it is concluded that because of the
presence of reciprocal connections between the postsubiculum and the ATN,
further studies are required in order to determine the direction in which
this head-directional information is flowing. Finally, ATN HD cells differ
from postsubicular HD cells by appearing to require volitional motoric
input.
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