The hippocampus and memory for orderly stimulus relations

Abstract

Human declarative memory involves a systematic organization of information that supports generalizations and inferences from acquired knowledge. This kind of memory depends on the hippocampal region in humans, but the extent to which animals also have declarative memory, and whether inferential expression of memory depends on the hippocampus in animals, remains a major challenge in cognitive neuroscience. To examine these issues, we used a test of transitive inference pioneered by Piaget to assess capacities for systematic organization of knowledge and logical inference in children. In our adaptation of the test, rats were trained on a set of four overlapping odor discrimination problems that could be encoded either separately or as a single representation of orderly relations among the odor stimuli. Normal rats learned the problems and demonstrated the relational memory organization through appropriate transitive inferences about items not presented together during training. By contrast, after disconnection of the hippocampus from either its cortical or subcortical pathway, rats succeeded in acquiring the separate discrimination problems but did not demonstrate transitive inference, indicating that they had failed to develop or could not inferentially express the orderly organization of the stimulus elements. These findings strongly support the view that the hippocampus mediates a general declarative memory capacity in animals, as it does in humans.

Figure 1

(A) Lateral reconstruction of the smallest (solid line) and largest (dashed line) of the PRER ablations; areas 35 and 36 collectively constitute the perirhinal cortex. This figure is based on coordinates used by Burwell, Amaral and Witter (24). (B) Coronal reconstruction of the FX transection (right hemisphere) and intact brain region (left hemisphere). (Figure based on ref. .)

Figure 2

(A) The mean number of trials required to reach the criterion for each phase of premise training. Error bars represent SE above the mean. (B) Mean response accuracy (±SE) on each of the four premise pairs during the test sessions.

Figure 3

(A) Mean response accuracy (+SE) for the average performance on premise pairs BC and CD and for the critical test pair BD during the test sessions. (B) Response accuracy (+SE) for control probe pair AE and the average response accuracy for the new control pairs (WX and YZ).