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The Journal of Neuroscience, January 28, 2009, 29(4):1061-1076; doi:10.1523/JNEUROSCI.1679-08.2009

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Behavioral/Systems/Cognitive
Head Direction Cell Activity in Mice: Robust Directional Signal Depends on Intact Otolith Organs

Ryan M. Yoder 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.s.taube{at}dartmouth.edu

The head direction (HD) cell signal is a representation of an animal's perceived directional heading with respect to its environment. This signal appears to originate in the vestibular system, which includes the semicircular canals and otolith organs. Preliminary studies indicate the semicircular canals provide a necessary component of the HD signal, but involvement of otolithic information in the HD signal has not been tested. The present study was designed to determine the otolithic contribution to the HD signal, as well as to compare HD cell activity of mice with that of rats. HD cell activity in the anterodorsal thalamus was assessed in wild-type C57BL/6J and otoconia-deficient tilted mice during locomotion within a cylinder containing a prominent visual landmark. HD cell firing properties in C57BL/6J mice were generally similar to those in rats. However, in C57BL/6J mice, landmark rotation failed to demonstrate dominant control of the HD signal in 36% of the sessions. In darkness, directional firing became unstable during 42% of the sessions, but landmark control was not associated with HD signal stability in darkness. HD cells were identified in tilted mice, but directional firing properties were not as robust as those of C57BL/6J mice. Most HD cells in tilted mice were controlled by landmark rotation but showed substantial signal degradation across trials. These results support current models that suggest otolithic information is involved in the perception of directional heading. Furthermore, compared with rats, the HD signal in mice appears to be less reliably anchored to prominent environmental cues.

Key words: otolith organs; mouse; gravity; anterodorsal thalamic nucleus; navigation; head direction

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Received Aug. 14, 2008; revised Dec. 16, 2008; accepted Dec. 17, 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.s.taube{at}dartmouth.edu

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				G. M. Muir, J. E. Brown, J. P. Carey, T. P. Hirvonen, C. C. Della Santina, L. B. Minor, and J. S. Taube Disruption of the Head Direction Cell Signal after Occlusion of the Semicircular Canals in the Freely Moving Chinchilla J. Neurosci., November 18, 2009; 29(46): 14521 - 14533. [Abstract] [Full Text] [PDF]

				M. Beraneck and F. M. Lambert Impaired Perception of Gravity Leads to Altered Head Direction Signals: What Can We Learn From Vestibular-Deficient Mice? J Neurophysiol, July 1, 2009; 102(1): 12 - 14. [Abstract] [Full Text] [PDF]

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