A cognitive map for object memory in the hippocampus

Abstract

The hippocampus has been proposed to support a cognitive map, a mental representation of the spatial layout of an environment as well as the nonspatial items encountered in that environment. In the present study, we recorded simultaneously from 43 to 61 hippocampal pyramidal cells as rats performed an object recognition memory task in which novel and repeated objects were encountered in different locations on a circular track. Multivariate analyses of the neural data indicated that information about object identity was represented secondarily to the primary information dimension of object location. In addition, the neural data related to performance on the recognition memory task. The results suggested that objects were represented as points of interest on the hippocampal cognitive map and that this map was useful in remembering encounters with particular objects in specific locations.

Figure 1.

Schematic of the recognition memory task procedure. Ten blocks of trials were completed in each recording session. On each block of trials, four objects (indicated by letters) were encountered in various locations as rats completed clockwise laps on a circular track. Each block started with an empty lap, and the numbers on the drawing of the empty lap indicate the o'clock positions in which objects were encountered.

Figure 2.

Performance on the recognition memory task. Duration of exploration is plotted for the first six encounters with each object. For the first three encounters, the object remained in the same location. (*) Indicates a statistically significant reduction in exploration between the first and second encounter with an object (see Results), presumably reflecting memory for the repeated object. Between the third and fourth encounter, the object was moved to a new location. (†) Indicates a statistically significant increase in exploration between the third and fourth encounter (see Results), presumably reflecting memory for the object and its previous location. Error bars, SEM across the four rats.

Figure 3.

Firing rates from four example neurons as a function of object location (top row) or object identity (bottom row). The four example neurons are taken from rats 1, 2, 3, and 4, respectively. Example neurons 1 and 3 are CA1 pyramidal neurons, and neurons 2 and 4 are CA3 pyramidal neurons. Separate one-way ANOVAs were conducted on the data to test for main effects of object location and for object identity. All four neurons showed a significant effect of location (Ps < 0.01), whereas only two showed a significant effect of object identity (Ps < 0.01), reflecting the lesser prominence of object coding observed across all cells (see text for details).

Figure 4.

Multivariate representation of hippocampal activity for each object encounter for one example session (rat 1; see Supplemental Fig. 1 for graphs for the other three rats). The three panels show the three possible parings of the first three principal components of the pattern of activity across 61 simultaneously recorded hippocampal pyramidal neurons. The data point for each encounter is depicted by both a letter (or symbol), which represents the identity of the specific object, and a color, which represents the position in which it was encountered on the circular track. Data points tended to cluster first by object location and then by object identity (see Results). It should be noted that principal components were used only for plotting purposes and that all analyses were performed on the raw data.

Figure 5.

Nearest neighbor classification accuracy for object identity. Accuracy is shown as the percentage of object encounters for which the multivariate data point was closest to the data point of another encounter with the same object. The left bar shows the accuracy when considering only objects in the same location. The right bar shows the accuracy when considering only objects encountered in a different location. The accuracy for objects in the same location was well above chance (indicated by a dashed line) but was not significantly above chance for objects in different locations (see Results). Error bars, SEM for the four rats.

Figure 6.

Average similarity of hippocampal representations of object encounter events. The similarity of hippocampal representations was represented as the average standardized distances between multivariate data points for each object encounter event and all other events in one of four categories: encounters with the same object in the same location, encounters with a different object in the same location, encounters with the same object in a different location, and encounters with a different object in a different location. Shorter distances indicate greater similarity of neural patterns. Encounters with the same object were more similar than encounters with different objects (* indicates a P-value less than 0.01 from a paired samples t-test) but only when the encounters were in the same location (n.s. indicates not statistically significant; P > 0.05; for full statistical analyses, see text). Error bars, SEM across the four rats.

Figure 7.

Similarity of hippocampal representations of object identity and object location for the first six encounters with an object. The similarity of hippocampal representations was represented as nearest neighbor distances between multivariate data points representing the pattern of neural activity across all simultaneously recorded cells (see Materials and Methods). Information about object location for each object encounter was calculated as the distance between the data point representing that encounter and the nearest data point representing an encounter in the same location (shown in blue). Information about object identity for each object encounter was calculated as the distance between the data point representing that encounter and the nearest data point representing an encounter with the same object in the same location (shown in red). (*) Indicates that nearest neighbor distances for object identity were significantly shorter for the first repetition of an object in the same location, reflecting a greater amount of object information for the second time it was encountered compared with the first time it was encountered. (†) Indicates that nearest neighbor distances for object location were significantly longer for the first encounter for an object repeated in a new location, reflecting a decreased amount of location information for the object's new location compared with the previous location. The overall shorter distances for object location compared with object identity reflects the primacy of location coding (see Results). Distances were converted to Z-scores for each session. Error bars, SEM across the four rats.