Failure of Centrally Placed Objects to Control the Firing Fields of Hippocampal Place Cells

Abstract

Previous work has shown that the angular position of hippocampal place cell firing fields is accurately controlled by the position of a single white cue card attached to the wall of a recording cylinder: when the card is rotated, fields rotate equally. In this study, we asked whether similar control could be exerted by three-dimensional objects placed directly in the recording arena. In each of several conditions, the locations of the objects relative to each other and their distances from the cylinder wall were fixed. In Experiment 1, the objects were all near the center of the cylinder. In this condition, the angular position of firing fields could, in general, not be predicted from the angular position of the object set. When a white wall card was added to the object arrangement, the stimulus ensemble exerted nearly ideal control over angular firing position. Nevertheless, when the card was withdrawn, the objects still did not control field position. In Experiment 2, place cells were recorded in the presence of two new arrangements of the same objects used in Experiment 1. In the "clustered objects" condition, the objects were placed next to each other, 10 cm from the wall. In the "objects-at-periphery" condition, the objects were put against the cylinder wall by equally increasing the distances among the objects. In both conditions, we found virtually ideal control by the objects over angular field position. These results indicate that the failure of stimulus control in Experiment 1 must be attributable to the arrangement of the objects and not to the nature of the objects themselves. Overall, the results are in line with behavioral studies that show that it is very difficult to teach rats to locate food relative to landmarks inside the behavioral arena.

Conjoint Control of Hippocampal Place Cell Firing by Two Visual Stimuli

“…Firing fields were otherwise unaltered by such rigid rotations. This nearly ideal control of firing fields by specific stimuli is also in agreement with previous work (O'Keefe and Conway 1978; Muller and Kubie 1987; Sharp et al 1990; Gothard et al 1996; Cressant et al 1997). (c) The only effect of removing one card and rotating the other was to cause uniform rotations of all firing fields.…”

Geometric determinants of human spatial memory

“…Firstly we note that, in rats, proximal visual landmarks have a much weaker effect on the orientation of the place cell representation than distal visual landmarks (Cressant et al, 1997). Thus, if behavior in reorientation paradigms depends on a similar system in humans, we would expect distant landmarks beyond the immediate environmental boundaries to reduce the incidence of disoriented responses.…”

“…For example, many manipulations do not affect the spatial firing fields of hippocampal place cells, including the removal of subsets of visual cues (O'Keefe & Conway, 1978) and the movement of small objects within the environment (Cressant, Muller, & Poucet, 1997). However, place fields can be distorted by changing the shape and size of the environment.…”

The hippocampal debate: are we asking the right questions?

“…These correlations (termed the place field of the cell) show many important properties, including appearing immediately upon entry into a novel area [79,241], following synchronous rotations of external cues [38,129,148], and continuing to show place fields in the absence of landmarks [129,152] and in the dark [100,166]. See [173] for review.…”