As a rat navigates through space, neurons known as Head Direction cells provide an ongoing indication of momentary directional heading. Each cell fires when the animal is facing one particular direction. Every cell has its own firing direction, so that each heading is signalled by activity in a unique subset of these cells. It is not clear how these signals are generated. Surprisingly, there is no evidence for geomagnetic influences. Rather, the cells are influenced, in part, by visual cues; salient visual landmarks can """"""""set"""""""" the darkness. Thus, the cells must also use cues which signal angular head motion (e.g., vestibular or visual motion cues) since, in the absence of landmarks, these are the only ongoing indicators of directional heading. Head Direction cells have been found in several interconnected brain regions, including the postsubiculm, retrosplenial cortex, laterodorsal thalamic nucleus, and anterior thalamic nuclei. These areas, in turn, are connected to several other regions, including the reticular thalamic nucleus, mammillary bodies, pretectal area and superior colliculus. Cells in the latter areas have not yet been examined for direction correlates. The goal of these studies is to examine each area in this circuit for the presence of cells (other than Head Direction cells themselves) which could constitute the building blocks for the head direction signal. Cells in each area will be recorded as animals navigate while performing a food pellet retrieving task. The animals will be equipped with two headlights, which provide a continual indication of the animal's momentary directional heading. Cell activity in each area will be examined for any directional, visual, or angular motion correlates. The sensory basis of any such signals will be examined in probe studies including 1) lights out sessions to test for visual influences. 2) passive rotation sessions, to test for dependence on the animal's own motor movements, and 3) delivery of experimenter-generated vestibular and visual motion cues. When completed, the proposed studies, along with earlier work, will provide a complete examination of the basic navigation related firing properties in the Head Direction cell circuit. This will provide a basis for development of a theoretical explanation for these cells. This is an important goal because 1) it will provide an example of how a neural circuit can generate a highly abstract representation (head direction), and 2) it will provide insight into one aspect of the overall set of cognitive and perceptual abilities involved in navigation.

Agency
National Institute of Health (NIH)
Institute
National Institute of Neurological Disorders and Stroke (NINDS)
Type
Research Project (R01)
Project #
1R01NS035191-01A1
Application #
2038296
Study Section
Special Emphasis Panel (ZRG2-BPO (01))
Program Officer
Baughman, Robert W
Project Start
1997-04-01
Project End
2000-03-31
Budget Start
1997-04-01
Budget End
1998-03-31
Support Year
1
Fiscal Year
1997
Total Cost
Indirect Cost
Name
Yale University
Department
Psychology
Type
Schools of Arts and Sciences
DUNS #
082359691
City
New Haven
State
CT
Country
United States
Zip Code
06520
Sharp, Patricia E; Koester, Kate (2008) Lesions of the mammillary body region alter hippocampal movement signals and theta frequency: implications for path integration models. Hippocampus 18:862-78
Sharp, Patricia E; Koester, Kate (2008) Lesions of the mammillary body region severely disrupt the cortical head direction, but not place cell signal. Hippocampus 18:766-84
Sharp, Patricia E; Turner-Williams, Shawnda; Tuttle, Sarah (2006) Movement-related correlates of single cell activity in the interpeduncular nucleus and habenula of the rat during a pellet-chasing task. Behav Brain Res 166:55-70
Bingman, Verner P; Sharp, Patricia E (2006) Neuronal implementation of hippocampal-mediated spatial behavior: a comparative evolutionary perspective. Behav Cogn Neurosci Rev 5:80-91
Sharp, Patricia E; Turner-Williams, S (2005) Movement-related correlates of single-cell activity in the medial mammillary nucleus of the rat during a pellet-chasing task. J Neurophysiol 94:1920-7
Sharp, P E; Blair, H T; Cho, J (2001) The anatomical and computational basis of the rat head-direction cell signal. Trends Neurosci 24:289-94
Sharp, P E; Tinkelman, A; Cho, J (2001) Angular velocity and head direction signals recorded from the dorsal tegmental nucleus of gudden in the rat: implications for path integration in the head direction cell circuit. Behav Neurosci 115:571-88
Cho, J; Sharp, P E (2001) Head direction, place, and movement correlates for cells in the rat retrosplenial cortex. Behav Neurosci 115:3-25
Blair, H T; Cho, J; Sharp, P E (1999) The anterior thalamic head-direction signal is abolished by bilateral but not unilateral lesions of the lateral mammillary nucleus. J Neurosci 19:6673-83
Blair, H T; Cho, J; Sharp, P E (1998) Role of the lateral mammillary nucleus in the rat head direction circuit: a combined single unit recording and lesion study. Neuron 21:1387-97