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Passive Transport Disrupts Directional Path Integration by Rat Head Direction Cells

Department of Psychological and Brain Sciences, Center for Cognitive Neuroscience, Dartmouth College, Hanover, New Hampshire 03755

Submitted 8 April 2003; accepted in final form 23 July 2003

A subset of neurons in the rat limbic system encodes head direction (HD) by selectively discharging when the rat points its head in a preferred direction in the horizontal plane. The preferred firing direction is sensitive to the location of landmark cues, as well as idiothetic or self-motion cues (i.e., vestibular, motor efference copy, proprioception, and optic flow). Previous studies have shown that the preferred firing direction remains relatively stable (average shift ± 18°) after the rat walks from a familiar environment into a novel one, suggesting that without familiar landmarks, the preferred firing direction can be maintained using idiothetic cues, a process called directional path integration. This study repeated this experiment and manipulated the idiothetic cues available to the rat as it moved between the familiar and novel environment. Motor efference copy/proprioceptive cues were disrupted by passively transporting the animal between the familiar and novel environment. Darkening the room as the animal moved to the novel environment eliminated optic flow cues. HD cell preferred firing directions shifted in the novel environment by an average of 30° after locomotion from the familiar environment with the room lights off; by an average of 70° after passive transport from the familiar environment with the room lights on; and by an average of 67° after passive transport with the room lights off. These findings are consistent with the view that motor efference copy/proprioception cues are important for maintaining the preferred firing direction of HD cells under conditions requiring path integration.

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