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Passive Movements of the Head Do Not Abolish Anticipatory Firing Properties of Head Direction Cells

¹Department of Psychological and Brain Sciences, Center for Cognitive Neuroscience, Dartmouth College, Hanover, New Hampshire; ²Centre National de la Recherche Scientifique, College de France, Laboratoire de Physiologie de la Perception et de l'Action, Paris, France; ³Medical Research Council Centre for Synaptic Plasticity, University of Bristol, Bristol, United Kingdom; and ⁴Department of Physiology, State University of New York, Downstate Medical Center, Brooklyn, New York

Submitted 19 May 2004; accepted in final form 27 September 2004

Neurons in the anterior dorsal thalamic nucleus (ADN) of the rat selectively discharge in relation to the animal's head direction (HD) in the horizontal plane. Temporal analyses of cell firing properties reveal that their discharge is optimally correlated with the animal's future directional heading by 24 ms. Among the hypotheses proposed to explain this property is that ADN HD cells are informed of future head movement via motor efference copy signals. One prediction of this hypothesis is that when the rat's head is moved passively, the anticipatory time interval (ATI) will be attenuated because the motor efference signal reflects only the active contribution to the movement. The present study tested this hypothesis by loosely restraining the animal and passively rotating it through the cell's preferred direction. Contrary to our prediction, we found that ATI values did not decrease during passive movement but in fact increased significantly. HD cells in the postsubiculum did not show the same effect, suggesting independence between the two sites with respect to anticipatory firing. We conclude that it is unlikely that a motor efference copy signal alone is responsible for generating anticipatory firing in ADN HD cells.

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