Edward J. Golob

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.

Recordings of postsubiculum head direction cells following lesions of the laterodorsal thalamic nucleus.

Areas of the rodent limbic system are important for solving spatial tasks and accurate navigation. Previous studies have identified cells in the postsubiculum (PoS) and the lateral dorsal thalamus (LDN) which discharge as a function of the animals head direction in the horizontal plane. These two brain areas are reciprocally connected with one another. To determine the contribution of the LDN to the functioning of PoS head direction cells, we lesioned the LDN and recorded single units in the PoS. We report here that lesions of the LDN had little effect upon the firing properties of PoS HD cells. In addition, HD cells from lesioned animals showed normal responses to two environmental manipulations: (1) when the salient visual cue was rotated the preferred firing directions of PoS HD cells shifted a similar amount and (2) cells frequently ceased firing, or had reductions in their peak firing rate, when the animal was restrained and passively rotated through the preferred firing direction. These results indicate that the LDN does not play a substantive role in either the generation or the stability of the HD cell signal in the PoS.

Differences between appetitive and aversive reinforcement on reorientation in a spatial working memory task.

Tasks using appetitive reinforcers show that following disorientation rats use the shape of an arena to reorient, and cannot distinguish two geometrically similar corners to obtain a reward, despite the presence of a prominent visual cue that provides information to differentiate the two corners. Other studies show that disorientation impairs performance on certain appetitive, but not aversive, tasks. This study evaluated whether rats would make similar geometric errors in a working memory task that used aversive reinforcement. We hypothesized that in a task that used aversive reinforcement rats that were initially disoriented would not reorient by arena shape and thus make similar geometric errors. Tests were performed in a rectangular arena having one polarizing cue. In the appetitive condition water consumption was the reward. The aversive condition was a water maze task with reinforcement provided by escape to a hidden platform. In the aversive condition rats returned to the reinforced corner significantly more often than in the dry condition, and did not favor the diagonally opposite corner. Results show that rats can use cues besides arena shape to reorient in an aversive reinforcement condition. These findings may also reflect different strategies, with an escape/homing strategy in the wet condition and a foraging strategy in the dry condition.

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.

Computational functions of the hippocampus: does it encode all episodic memories?

Recent neurophysiological results in animals with hippocampal lesions challenge the notion that the hippocampus is required for encoding all forms of episodic memories.