One cognitive function often taken for granted is the ability to maintain a sense of direction and location while moving about in the environment. This awareness is essential for getting around and functioning normally in the world. When our sense of spatial orientation is compromised by central nervous system or vestibular disease, the seriousness and devastation of the disorder becomes readily apparent both to the patient and clinician. Common problems include dizziness, balance, and spatial disorientation. To develop effective treatments for these disorders, we will need to understand the neural processes underlying spatial orientation and what goes awry with these processes that brings about disorientation. Thus, the long-term goal of this proposal is to better understand the neural mechanisms contributing to spatial perception of one's orientation. Using an animal model and electrophysiological techniques we will record from a class of neurons in rats that encodes the animal's directional heading in allocentric coordinates. These neurons are referred to as 'head direction (HD) cells'and have been identified in non-human primates.
Our aim i s to understand how head direction cells respond under a variety of conditions that pertain to issues of spatial orientation and disorientation. The experiments investigate 1) the response of HD cells in three dimensions - in particular, how they respond when the animal is inverted and locomotes upside-down while performing a spatial memory task, 2) the role of the vestibular system, both the semi-circular canals and the otolith organs, in generating HD cell responses, 3) the role of motor/proprioceptive cues in the discharge of angular head velocity cells, 4) the role of limbic system circuitry in generating head direction cell responses in the striatum, and 5) the response of HD cells during periods of disorientation. In sum, the results we obtain will provide essential information for understanding the neurophysiological basis for spatial orientation disorientation, and enhance our understanding of how spatial information is organized and processed in the mammalian brain.

Public Health Relevance

The results from these experiments will provide key information in understanding the basic neural mechanisms underlying spatial orientation. Ultimately, we would like to develop a better neurophysiological understanding of disorientation and use this information to develop effective treatments for spatial disorders such as vertigo, motion sickness, navigational disorders. Further, it is common for patients with vestibular disorders, elderly patients, and patients with Alzheimer's disease, a disease often associated with marked pathology in limbic system structures, to experience spatial disorientation to the extent that constant supervision is required. Learning how spatial information is processed in the rat brain will provide clues about the complex nature of spatial processes in humans.

Agency
National Institute of Health (NIH)
Institute
National Institute on Deafness and Other Communication Disorders (NIDCD)
Type
Research Project (R01)
Project #
5R01DC009318-04
Application #
8080814
Study Section
Special Emphasis Panel (ZRG1-IFCN-A (05))
Program Officer
Platt, Christopher
Project Start
2008-07-01
Project End
2013-06-30
Budget Start
2011-07-01
Budget End
2013-06-30
Support Year
4
Fiscal Year
2011
Total Cost
$293,062
Indirect Cost
Name
Dartmouth College
Department
Psychology
Type
Schools of Arts and Sciences
DUNS #
041027822
City
Hanover
State
NH
Country
United States
Zip Code
03755
Valerio, Stephane; Taube, Jeffrey S (2016) Head Direction Cell Activity Is Absent in Mice without the Horizontal Semicircular Canals. J Neurosci 36:741-54
Shinder, M E; Taube, J S (2014) Resolving the active versus passive conundrum for head direction cells. Neuroscience 270:123-38
Shinder, Michael E; Taube, Jeffrey S (2014) Self-motion improves head direction cell tuning. J Neurophysiol 111:2479-92
Clark, Benjamin J; Rice, James P; Akers, Katherine G et al. (2013) Lesions of the dorsal tegmental nuclei disrupt control of navigation by distal landmarks in cued, directional, and place variants of the Morris water task. Behav Neurosci 127:566-81
Gibson, Brett; Butler, William N; Taube, Jeffery S (2013) The head-direction signal is critical for navigation requiring a cognitive map but not for learning a spatial habit. Curr Biol 23:1536-40
Taube, Jeffrey S; Valerio, Stephane; Yoder, Ryan M (2013) Is navigation in virtual reality with FMRI really navigation? J Cogn Neurosci 25:1008-19
Taube, Jeffrey S; Shinder, Michael (2013) On the nature of three-dimensional encoding in the cognitive map: Commentary on Hayman, Verriotis, Jovalekic, Fenton, and Jeffery. Hippocampus 23:14-21
Valerio, Stephane; Taube, Jeffrey S (2012) Path integration: how the head direction signal maintains and corrects spatial orientation. Nat Neurosci 15:1445-53
Clark, Benjamin J; Brown, Joel E; Taube, Jeffrey S (2012) Head direction cell activity in the anterodorsal thalamus requires intact supragenual nuclei. J Neurophysiol 108:2767-84
Yoder, Ryan M; Taube, Jeffrey S (2011) Projections to the anterodorsal thalamus and lateral mammillary nuclei arise from different cell populations within the postsubiculum: implications for the control of head direction cells. Hippocampus 21:1062-73

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