Rat anterodorsal thalamic head direction neurons depend upon dynamic visual signals to select anchoring landmark cues

Abstract

Head direction cells, which are functionally coupled to 'place' cells of the hippocampus, a structure critically involved in spatial cognition, are likely neural substrates for the sense of direction. Here we studied the mechanism by which head direction cells are principally anchored to background visual cues [M.B. Zugaro et al. (2001) J. Neurosci., 21, RC154,1-5]. Anterodorsal thalamic head direction cells were recorded while the rat foraged on a small elevated platform in a 3-m diameter cylindrical enclosure. A large card was placed in the background, near the curtain, and a smaller card was placed in the foreground, near the platform. The cards were identically marked, proportionally dimensioned, subtended the same visual angles from the central vantage point and separated by 90 degrees. The rat was then disoriented in darkness, the cards were rotated by 90 degrees in opposite directions about the center and the rat was returned. Preferred directions followed either the background card, foreground card or midpoint between the two cards. In continuous lighting, preferred directions shifted to follow the background cue in most cases (30 of the 53 experiments, Batschelet V-test, P < 0.01). Stroboscopic illumination, which perturbs dynamic visual signals (e.g. motion parallax), blocked this selectivity. Head direction cells remained equally anchored to the background card, foreground card or configuration of the two cards (Watson test, P > 0.1). This shows that dynamic visual signals are critical in distinguishing typically more stable background cues which govern spatial neuronal responses and orientation behaviors.

Head Direction Cell Representations Maintain Internal Coherence during Conflicting Proximal and Distal Cue Rotations: Comparison with Hippocampal Place Cells

“…Thus, in these datasets, it is unlikely that the place cells and head direction cell tuning curves showed proximal cue control strictly by chance. Rather, the proximal cues exerted a relatively weak, but significant, effect on the head direction ensemble, consistent with a previous report that the head direction cell orientation can be controlled by the orientation of a T-maze (Dudchenko et al, 2005) (see also Zugaro et al, 2004).…”

Spatial reorientation in large and small enclosures: comparative and developmental perspectives

“…Data on the importance of distal cues also come from neurobiological experiments (Zugaro et al 2004). Rats underwent tests in an enclosure in which orienting cues were provided by the presence of a foreground (proximal) and a background (distal) card.…”

Weighted cue integration in the rodent head direction system

“…Each HD cell is tuned to a single head orientation, and when the head is directed to the cell's preferred firing direction the cell fires at maximum [1]. Many studies have illustrated that the HD system is strongly reliant on external landmark cues in order to determine heading direction [3][4][5]. However, this reliance is variable, depending upon the type of external cue, the location of that cue in the environment, the prior experience of the cue and the duration of exposure to it.…”