Contrasting effects on discrimination learning after hippocampal lesions and conjoint hippocampal-caudate lesions in monkeys

Abstract

Eighteen monkeys with lesions of the hippocampal region (the hippocampus proper, the dentate gyrus, and the subiculum) made by an ischemic procedure, radio frequency, or ibotenic acid were tested on a simple, two-choice object discrimination learning task that has been shown to be sensitive to large lesions of the medial temporal lobe. The monkeys were also tested on two other discrimination tasks (pattern discrimination and eight-pair concurrent discrimination) that can be learned normally by monkeys with large medial temporal lobe lesions. All of the lesion groups were impaired at learning the simple object discrimination task. Seven of the monkeys who had sustained damage to the hippocampal region also sustained damage to the tail of the caudate nucleus. These seven monkeys, but not the other 11 monkeys with hippocampal lesions, were impaired on pattern discrimination and concurrent discrimination learning. The results suggest that the hippocampal region is important for learning easy, two-choice discriminations, whereas the caudate nucleus is necessary for the normal learning of more difficult, gradually acquired discrimination tasks. The findings support the distinction between declarative memory, which depends on the hippocampus and related medial temporal lobe structures, and habit learning, which depends on the caudate nucleus.

Fig. 1.

Photomicrographs of thionin-stained sections through two levels of the left and right temporal lobe of a normal monkey (A) and a representative monkey from the ISC (B), RF1 (C), RF2 (D), and IBO1 (E) groups. Scale bar (in A): A–E, 2 mm.

Fig. 2.

Performance on the simple object discrimination learning task. A, Learning curves (in blocks of 4 trials) for 18 monkeys with lesions of the hippocampal region (H,filled circles) and 16 normal monkeys (N, open circles) across the 3 test days. Performance scores have been averaged across four separate object discrimination tasks. Range of SEs: group N, 0.012–0.033; group H, 0.013–0.028.B, Mean percent correct scores for the first four trials of testing of each day for the H (filled bars) and the N (open bars) groups. The 18 monkeys in the H group consist of four monkeys with ischemic lesions (ISC), nine monkeys with radio frequency lesions (RF1 and RF2), and five monkeys with ibotenate lesions (IBO1). C, Mean percent correct scores for the first four trials of testing of each day for nine amnesic patients (filled bars) and 14 controls (open bars) (from Squire et al., 1988). For the humans, the scores are the averages from three separate object discrimination tasks. For B and C,brackets show SEM. *p < 0.05.

Fig. 3.

Performance on the pattern discrimination task for 16 normal control monkeys (N), 11 monkeys with lesions of the hippocampal region (H), and seven monkeys with lesions of the hippocampal region that included substantial damage to the tail of the caudate nucleus (H-Cd). The 11 monkeys in the H group consist of four monkeys with ischemic lesions (ISC), two monkeys with radio frequency lesions (RF1–3 and RF1–4), and five monkeys with ibotenate lesions (IBO1). The seven monkeys in the H-Cd group all had radio frequency lesions (RF1–1, RF1–2, and the 5 monkeys in the RF2 group). Performance scores for the two pattern discrimination problems are averaged together. Symbolsshow the performance of individual monkeys.

Fig. 4.

Performance on the concurrent discrimination task for 16 normal control monkeys (N), 11 monkeys with lesions of the hippocampal region (H), and seven monkeys with lesions of the hippocampal region that included substantial damage to the tail of the caudate nucleus (H-Cd). See Figure 3 for the composition of the two lesion groups. Symbols show the performance of individual monkeys.