Jeremy P. Goodridge

Cue control and head direction cells

Previous research has shown that head direction (HD) cells in both the anterior dorsal thalamus (ADN) and the postsubiculum (PoS) in rats discharge in relation to familiar, visual landmarks in the environment. This study assessed whether PoS and ADN HD cells would be similarly responsive to nonvisual or unfamiliar environmental cues. After visual input was eliminated by blindfolding the rats, HD cells maintained direction-specific discharge, but their preferred firing directions became less stable. In addition, rotations of the behavioral apparatus indicated that some nonvisual cues (presumably tactile, olfactory, or both) exerted above chance stimulus control over a cells preferred firing direction. However, a prominent auditory cue was not effective in exerting stimulus control over a cells preferred direction. HD cell activity also was assessed after rotation of a novel visual cue exposed to the rat for 1, 3, or 8 min. An 8-min exposure was enough time for a novel visual cue to gain control over a cells preferred direction, whereas an exposure of 1 or 3 min led to control in only about half the sessions. These latter results indicate that HD cells rely on a rapid learning mechanism to develop associations with landmark cues.

Processing the head direction cell signal: A review and commentary

Animals require information about their location and directional heading in order to navigate. Directional information is provided by a population of cells in the postsubiculum and the anterior thalamic nuclei that encode a very accurate, continual representation of the animals directional heading in the horizontal plane, which is independent of the animals location. Recent studies indicate that this signal 1) arises either in the anterior thalamic nuclei or in structures upstream from it; 2) is not dependent on an intact hippocampus; 3) receives sensory inputs from both idiothetic and landmark systems; and 4) correlates well with the animals behavior in a spatial reference memory task. Furthermore, HD cells in the anterior thalamic nuclei appear to encode what the animals directional heading will be about 40 ms in the future, while HD cells in the postsubiculum encode the animals current directional heading. Both the electrophysiological and anatomical data suggest that the anterior thalamic nuclei and/or the lateral mammillary nuclei may be the sites of convergence for spatial information derived from landmarks and internally-generated cues. Current evidence also indicates that the vestibular system plays a crucial role in the generation of the HD cell signal. However, the notion that the vestibular system is the sole contributor to the signal generator is difficult to reconcile with several findings; these latter findings are better accounted for with a motor efference copy signal.

Preferential use of the landmark navigational system by head direction cells in rats

Previous studies have identified a population of cells recorded in the postsubiculum and the anterior thalamic nucleus (ATN) that discharge as a function of an animals head direction (HD) in the horizontal plane. The present experiments monitored HD cell activity when rats were confronted with a situation in which directional information from internal sensory sources (e.g., proprioceptive, vestibular, or motor efference copy) conflicted with directional information derived from familiar, external landmarks. Results showed that when a salient, familiar cue was reintroduced to rats environment into a position that conflicted with the cells current firing direction, HD cells in both the ATN and the postsubiculum shifted their preferred direction to reflect their originally established orientation with this cue. This finding suggests that sensory inputs onto HD cells from external landmark cues are capable of overriding spatial information developed through internal sensory cues.

Effects of Repeated Disorientation on the Acquisition of Spatial Tasks in Rats: Dissociation Between the Appetitive Radial Arm Maze and Aversive Water Maze

This study examined the effects of disorientation on the acquisition of different spatial reference memory tasks. In an appetitively motivated radial arm maze task in which 1 arm was consistently baited, rats that were disoriented before each trial were impaired in their ability to acquire the task relative to rats placed in a clear container and not disoriented. However, disoriented rats were able to learn a Morris water maze and a water version of the radial arm maze under similar training conditions, suggesting that the effects of disorientation may interact with the quality or quantity of motivation involved in a given task. These results suggest that appetitive and aversive spatial tasks are dissociable, and that any impairment that is due to disorientation is specific to the appetitive radial arm maze task.

The effects of disorientation on visual landmark control of head direction cell orientation

Abstract Head direction (HD) and place cells were recorded in rats that had previously exhibited significant acquisition deficits on a radial arm maze task following disorientation treatment. In this study we determined whether this behavioral impairment was associated with a lack of landmark stimulus control over the preferred orientations of HD and place cells. Neurons were recorded as animals retrieved food pellets in a cylindrical apparatus containing a single cue card. Some of these HD cells were also recorded while animals explored an eight-arm radial maze in a similar cue-controlled environment. The stimulus control of the landmarks in each environment was assessed by rotating the landmark and examining the subsequent preferred orientations of HD and place cells. Animals underwent disorientation treatment before and after each recording session. Despite this disorientation, rotation of the cue card in the cylindrical apparatus resulted in a corresponding shift in the preferred orientations of HD and place cells in 13 of 15 and 7 of 7 recording sessions, respectively. On the radial arm maze, rotation of the landmark cue was associated with a corresponding shift in the HD cell’s preferred orientation in 7 of 9 sessions. These results suggest that a visual landmark’s stimulus control may not require a learned association between that landmark and an animal’s stable experience in an environment. Furthermore, instability in the HD cell system is unlikely to account for the impaired performance of the disoriented animals in the radial arm maze. Rather, these impairments may be due to the animal’s inability to utilize stable representations of the environment provided by HD and place cells.

A model of the rodent head direction system that accounts for unique properties of anterior thalamic head direction cells

Abstract We present a model of the rat head direction cell circuit that accounts for the recently discovered bimodality and distortion observed in the tuning curves of anterior thalamic head direction cells. This model also explains why anterior thalamic head direction cells show a constant amount of anticipation across all angular velocities.

Path integration in the rat head-direction circuit

As a rat navigates through space, neurons called head-direction (HD) cells provide an ongoing signal of the animal’s directional heading in the horizontal plane1,2. It is believed that the population of HD cells may function as a neural compass, providing the rat with its sense of direction during spatial navigation. The HD cell signal is thought to be generated, in part, by a path integration mechanism that uses angular motion information to compute the rat’s directional heading3–5. Here we review empirical findings that suggest how different brain regions might participate in this process of angular path integration.