[Neural basis for spatial memory in animals: what do hippocampal neurons tell us?]. / Les bases neurales de la mémoire spatiale chez l'animal: que nous disent les neurones de l'hippocampe?

Recent studies relying on the recording of neuronal unit activity in freely moving rats show the existence of two populations of neurons signalling the animal's location or head direction: place cells found primarily in the hippocampus and head direction cells found in brain areas anatomically and functionally related to the hippocampus. The properties of these two neuronal populations suggest that their activity strongly depends upon information cues stemming from the spatial environment, and also suggest their involvement in spatial memory. Place cells and head direction cells would jointly participate in a neural network allowing the animal to orient in space and to store spatial locations in memory. This network would also be operating in humans, in particular for encoding specific events in episodic memory.

Is the hippocampus of the rat part of a specialized navigational system?

The spatial mapping theory of hippocampal function proposes that the rat hippocampus is specialized for navigational computations, computations that allow the animal to solve difficult spatial problems. In this paper, we review evidence obtained by recording place cells and other "spatially tuned" cells from freely moving rats. Our main conclusion is that the nature of the signals carried by these cells and the ways in which the signals transform after changing the environment imply that the hippocampus and associated structures are able to represent aspects of the geometry of the environment.

Further study of the control of place cell firing by intra-apparatus objects.

The angular positions of hippocampal place cell firing fields are accurately controlled by the position of a single salient cue card attached to the wall of a recording cylinder; when the card is rotated, fields rotate equally. In contrast, the control exerted by 3-dimensional objects placed directly in the recording arena depends on their arrangement. When three objects lie on the vertices of an isosceles triangle near the center of the cylinder they rarely exert any control over the angular positions of firing fields. However, if the isosceles triangle is dilated so that its vertices are against the apparatus wall, the objects exert virtually ideal control over angular field position. Why do the objects gain control when they are against the cylinder wall? One possibility is that the asymmetry in the object set is more easily detected when the objects are far apart so that they provide a better polarizing cue. This hypothesis assumes that the identity of individual landmarks is not recognized by the place cell system whereas their geometric arrangement provides crucial information for controlling place field positions. If this is true, putting the 3 objects against the cylinder wall on the vertices of an equilateral triangle should cause a loss of stimulus control over the angular positions of firing fields. To the contrary, we found that the firing fields of most place cells (23/29) were accurately controlled by the equilateral object arrangement. Moreover, 5/6 of the uncontrolled cells were in a single animal. These results bolster our previous suggestion that the centrally placed objects fail to control place field positions because the computations necessary to form a stable reference frame are very difficult when the animal can go between stimuli.

Spatial firing of hippocampal place cells in blind rats.

The rat hippocampus contains cells that are characterized by location-specific firing. Previous work has shown that the angular position of hippocampal place cell firing fields is accurately controlled by the position of visual cues, suggesting that vision plays a important role in triggering place cell activity. However, a role for other types of information has also been suggested because place cell activity can be recorded while animals are moving in the darkness. In this study, we asked whether place fields can get established in rats that have never seen their environment. We studied place cell activity in early blind rats and found that these rats had place cells very similar to those recorded from sighted rats. This result suggests that early vision is not necessary for normal firing of hippocampal place cells. Dynamic, motion-related information in conjunction with stimulus recognition seems to be sufficient.

Failure of centrally placed objects to control the firing fields of hippocampal place cells.

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.