Impaired recognition memory in monkeys after damage limited to the hippocampal region

Abstract

Monkeys with lesions limited to the hippocampal region (the hippocampus proper, the dentate gyrus, and the subiculum) were impaired on two tasks of recognition memory: delayed nonmatching to sample and the visual paired-comparison task. Recognition memory was impaired in five different groups of monkeys, whether the lesions were made by an ischemic procedure, by radio frequency, or by ibotenic acid. The finding that the hippocampal region is essential for normal recognition memory performance is considered in the context of current ideas about the role of the hippocampus in declarative memory.

Fig. 1.

Group IBO1. Line drawings of representative coronal sections through the temporal lobe of M. fascicularis adapted from the atlas of Szabo and Cowan (1984). The sections are arranged from rostral (A15.5) to caudal (A3.6). The designations A15.5,A13.4, and so on specify distances anterior to the intra-aural line in millimeters. The extent of the lesions of the hippocampal region in each of the five monkeys in the IBO1 group is plotted on the coronal sections. In each case, the area of the lesion is indicated in gray.

Fig. 2.

Photomicrographs of thionin-stained sections through the left and right temporal lobe of monkey IBO1-2, whose lesion approximated the intended lesion. The sections are arranged from rostral (A) to caudal (F) and correspond to the line drawings in Figure 1. Scale bar (shown in A forA–F): 2 mm.

Fig. 3.

Group IBO2. The extent of the lesions of the hippocampal region in each of the four monkeys in the IBO2 group is indicated in gray on the coronal sections. Sections are arranged as in Figure 1.

Fig. 4.

Photomicrographs of thionin-stained sections through the left and right temporal lobe of monkey IBO2-1, whose lesion approximated the intended lesion. The sections are arranged from rostral (A) to caudal (F) and correspond to the line drawings in Figure 3. Scale bar (shown inA for A–F): 2 mm.

Fig. 5.

Group RF2. The extent of the lesions of the hippocampal region in each of the four monkeys in the RF2 group is indicated in gray on the coronal sections. Sections arranged as in Figure 1.

Fig. 6.

Photomicrographs of thionin-stained sections through the left and right temporal lobe of monkey RF2-5, whose lesion approximated the intended lesion. The sections are arranged from rostral (A) to caudal (F) and correspond to the line drawings in Figure 5. Scale bar (shown inA for A–F): 2 mm.

Fig. 7.

Delayed nonmatching to sample performance of normal monkeys (N) and monkeys with lesions limited to the hippocampal region (the dentate gyrus, the cell fields of the hippocampus, and the subiculum) made by ischemia (ISC), radio frequency (RF1,RF2), or ibotenic acid (IBO1).Asterisks indicate impaired performance of the lesion group relative to the N group (p < 0.05). The RF1 group performed numerically worse than the N group at the 10 min delay, but the difference fell short of significance (p < 0.07). Parenthesesindicate the number of monkeys in each group. The four lesion groups were similarly impaired.

Fig. 8.

Visual paired-comparison performance of normal monkeys (same as in Fig. 7, N) and monkeys with radio-frequency (RF2) lesions or ibotenic acid (IBO2) lesions limited to the hippocampal region.Asterisks indicate impaired performance of the lesion group relative to the N group.Parentheses indicate the number of monkeys in each group. Brackets indicate SEM. The two lesion groups were similarly impaired.

Fig. 9.

Performance on the delayed nonmatching to sample task (left panel) and on the visual paired-comparison task (right panel) by all the monkeys in the current study with lesions limited to the hippocampal region. All the normal monkeys (N) that have been tested previously in our laboratory on these two tasks are also included. Asterisks indicate impaired performance of the lesion group relative to the N group.Parentheses indicate the number of monkeys in each group. ^aThe ISC monkeys were not tested at the 40 sec delay so that the scores of 14 monkeys contributed to this data point.