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The Journal of Neuroscience, January 14, 2009, 29(2):493-507; doi:10.1523/JNEUROSCI.2811-08.2009

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Behavioral/Systems/Cognitive
Head Direction Cell Instability in the Anterior Dorsal Thalamus after Lesions of the Interpeduncular Nucleus

Benjamin J. Clark, Asha Sarma, and Jeffrey S. Taube

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

Correspondence should be addressed to Jeffrey S. Taube, Department of Psychological and Brain Sciences, Dartmouth College, 6207 Moore Hall, Hanover, NH 03755. Email: jeffrey.taube{at}dartmouth.edu

Previous research has identified a population of cells throughout the limbic system that discharge as a function of the animal's head direction (HD). Altering normal motor cues can alter the HD cell responses and disrupt the updating of their preferred firing directions, thus suggesting that motor cues contribute to processing the HD signal. A pathway that conveys motor information may stem from the interpeduncular nucleus (IPN), a brain region that has reciprocal connections with HD cell circuitry. To test this hypothesis, we produced electrolytic or neurotoxic lesions of the IPN and recorded HD cells in the anterior dorsal thalamus (ADN) of rats. Direction-specific firing remained present in the ADN after lesions of the IPN, but measures of HD cell properties showed that cells had reduced peak firing rates, large directional firing ranges, and firing that predicted the animal's future heading more than in intact controls. Furthermore, preferred firing directions were moderately less influenced by rotation of a salient visual landmark. Finally, the preferred directions of cells in lesioned rats exhibited large shifts when the animals foraged for scattered food pellets in a darkened environment and when locomoting from a familiar environment to a novel one. We propose that the IPN contributes motor information about the animal's movements to the HD cell circuitry. Furthermore, these results suggest that the IPN plays a broad role in the discharge properties and stability of direction-specific activity in the HD cell circuit.

Key words: head direction cells; interpeduncular nucleus; lateral habenula; medial habenula; anterodorsal thalamic nucleus; spatial orientation; rat; navigation

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Received June 19, 2008; revised Nov. 30, 2008; accepted Dec. 1, 2008.

Correspondence should be addressed to Jeffrey S. Taube, Department of Psychological and Brain Sciences, Dartmouth College, 6207 Moore Hall, Hanover, NH 03755. Email: jeffrey.taube{at}dartmouth.edu

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Interpreting lesion effects on head direction anticipation

Matthijs A. A. van der Meer

J. Neurosci. Online, 15 Jan 2009 [Full text]

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