Contrasting effects on path integration after hippocampal damage in humans and rats

Abstract

The hippocampus and other medial temporal lobe structures have been linked to both memory and spatial cognition, but it has been unclear how these ideas are connected. We carried out parallel studies of path integration in patients with medial temporal lobe lesions and rats with hippocampal lesions. Subjects entered a circular arena without vision, searched for a target, and then attempted to return to the start location. Patients performed accurately, and as well as controls, so long as the outward path was relatively direct and the target was found within 20 s. In sharp contrast, rats with hippocampal lesions were impaired, even when the outward path was shorter than 1 m, involved no turns, and the target was found within 3 s. We suggest that patients succeeded because performance could be supported by working memory and that patients and rats differ after hippocampal lesions in their ability to construct a coherent working memory of spatial environments.

Fig. 1.

Experiment 1: Path integration by memory-impaired patients (MTL) and CON. (A) Performance as a function of the distance traveled to find the tile. When participants were disoriented by rotation (squares), they were no longer able to rely on self-motion cues and failed to path integrate. (B) Performance as a function of the time taken to find the tile. (C) Performance as a function of the number of turns made to find the tile. The dotted line indicates chance performance (90° error). *Denotes above-chance performance. Brackets show SEM.

Fig. 2.

Experiment 2: Path integration by H group rats (H) and CON. The error in the return path was measured by which box the animal first returned to (start box = 0; the two boxes immediately adjacent to the start box = 1; the two boxes 90° removed from the start box = 2; the two boxes 135° removed from the start box = 3; the box 180° from the start box = 4). (A) Performance as a function of the distance traveled to find the food. (B) Performance as a function of the time taken to find the food. (C) Performance as a function of the number of turns made to find the food. The dotted line indicates chance performance. *Denotes group difference, P < 0.05. Brackets show SEM.

Fig. 3.

Reconstruction of coronal sections at four anteroposterior levels through the hippocampus showing the smallest (black) and largest (gray) lesion. Numbers to the right of each section represent the distance (in millimeters) posterior to Bregma. The upper left section is the most anterior section and the lower right section is the most posterior section.