One-trial memory for object-place associations after separate lesions of hippocampus and posterior parahippocampal region in the monkey

Abstract

In earlier studies of one-trial spatial memory in monkeys (Parkinson et al., 1988; Angeli et al., 1993), severe and chronic memory impairment for both object-place association and place alone was found after ablation of the hippocampal formation. The results appeared to provide the first clear-cut evidence in the monkey of the essential role of the hippocampus in spatial memory, but that interpretation neglected the inclusion in the lesion of the underlying posterior parahippocampal region. To determine the separate contributions of the hippocampus and posterior parahippocampal region to these spatial forms of one-trial memory, we trained 10 rhesus monkeys, as before, to remember the spatial positions of either two different trial-unique objects overlying two of the wells in a three-well test tray (object-place trials) or simply two of the three wells (place trials). Six of the monkeys then received ibotenic acid lesions restricted to the hippocampal formation (group H), and the four others received selective ablations of the posterior parahippocampal region (group P), comprising mainly parahippocampal cortex, parasubiculum, and presubiculum. Group H was found to be completely unaffected postoperatively on both types of trials, whereas group P sustained an impairment on both types equal in magnitude to that observed after the combined lesions in the original studies. Thus, contrary to the previous interpretation, one-trial memory for object-place association and, perhaps more fundamentally, one-trial memory for two different places appear to be critically dependent not on the hippocampal formation but rather on the posterior parahippocampal region.

Fig. 1.

One-trial object-place association task. This figure shows a schematic drawing of the final stage of the task, in which an unlike pair of unbaited objects was presented in the sample phase. In the test phase, one of the two sample objects together with its exact duplicate were presented either over the same two food wells that were used in acquisition (OBJECT-PLACE TRIALS) or over one of the food wells used for acquisition and over the third, previously unused food well (PLACE TRIALS). Twelve of each trial type were intermixed within a session.ITI, Intertrial interval.

Fig. 2.

Intended lesion of the hippocampal formation (left column) and actual lesions in two representative cases (H4 and H6; middleand right columns, respectively) transferred to standard coronal sections. Numerals indicate distance in millimeters from the interaural vertical plane.

Fig. 3.

Intended lesion of the posterior parahippocampal region is in black. Numerals indicate distance in millimeters from the interaural vertical plane.PPS, Parasubiculum/presubiculum; PS, presubiculum; ERh, entorhinal cortex;PRh, perirhinal cortex; TH,TF, parahippocampal cortical areas (von Bonin and Bailey, 1947); TE, TEO, visual cortical areas (von Bonin and Bailey, 1947).

Fig. 4.

Intended lesion of the posterior parahippocampal region (left column) and actual lesions in two cases (P2 and P4; middle andright columns, respectively) transferred to standard coronal sections and reconstructed on standard ventral surface views (top). Note sparing of presubicular cortex in case P4.Numerals indicate distance in millimeters from the interaural vertical plane.

Fig. 5.

Photomicrographs of coronal sections through the hippocampal lesion in the right hemisphere of case H5. Middle section shows complete cell loss in the hippocampal formation, whereas the others show partial sparing of the hippocampal formation in the area medial to (i.e., to the left of) eacharrow. Left, middle, andright sections correspond to sections +13, +7, and +1 in Figure 2.

Fig. 6.

Preoperative baseline and postoperative performance on one-trial object-place association task. Each data point represents average score for a block of five daily sessions (120 trials). H, Monkeys with excitotoxic lesions of the hippocampal formation; P, monkeys with ablations of the posterior parahippocampal region; H-Asp, monkeys with hippocampectomy by aspiration that sustained combined damage to the hippocampus and posterior parahippocampal region in the study byParkinson et al. (1988).