COMPUTATIONAL BASIS OF THE HEAD DIRECTION CELL SIGNAL

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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.