When recognition memory is independent of hippocampal function

Abstract

Hippocampal damage has been thought to result in broad memory impairment. Recent studies in humans, however, have raised the possibility that recognition memory for faces might be spared. In five experiments we investigated face recognition in patients with hippocampal lesions (H) or large medial temporal lobe (MTL) lesions, including patients where neurohistological information was available. Recognition of novel faces was unequivocally intact in H patients but only at a short retention interval. Recognition memory for words, buildings, inverted faces, and famous faces was impaired. For MTL patients, recognition memory was impaired for all materials and across all retention intervals. These results indicate that structures other than the hippocampus, perhaps the perirhinal cortex, can support face recognition memory in H patients under some conditions. The fact that the faces were novel when recognition memory was intact does not fully account for our findings. We propose that the role of the hippocampus in recognition memory is related to how recognition decisions are accomplished. In typical recognition tasks, participants proceed by forming an association between a study item and the study list, and the recognition decision is later made based on whether participants believe the item was on the study list. We suggest that face recognition is an exception to this principle and that, at short retention intervals, participants can make their recognition decisions without making explicit reference to the study list. Important features of faces that might make face recognition exceptional are that they are processed holistically and are difficult to verbally label.

Keywords: amnesia; long-term memory.

Fig. 1.

Exp. 1. Performance of a control group (CON; black bars) and memory-impaired patients with damage limited to the hippocampus (H; white bars) or larger lesions of the MTL (gray bars) on two versions of the Words and Faces test (RMT) (17). Testing occurred either immediately after study (IMMED) or 1 d later (24 HR). (Left) Patients whose lesions have been characterized by postmortem histology. (Right) Patients whose lesions were estimated from quantitative structural neuroimaging. For H patients, memory for faces was intact when tested immediately after study but impaired when tested the next day. Memory for words was impaired regardless of the retention interval. MTL patients (EP on the left, GP on the right) were impaired in all conditions. Asterisks indicate a significant difference between patients and controls (*P < 0.05). Brackets indicate SEM.

Fig. 2.

Exp. 2. Recognition memory for faces, buildings, and words for a control group (CON; black bars) and for memory-impaired patients with damage limited to the hippocampus (H; white bars) or larger lesions of the MTL (gray bars). After studying a list of items (80 faces, 80 buildings, or 160 words), memory was tested immediately (IMMED), 15 min, 2 h, and 24 h later. The MTL patient was tested only at the immediate and 15-min retention test. Each test involved 20 old and 20 new faces or buildings (or 40 old and 40 new words). For faces, H patients performed as well as the CON group when tested immediately after study but were impaired on the delay tests (3 DELAYS: the mean score for the 15 min, 2 h, and 24 h retention tests). For buildings and words, the patients were impaired in all conditions tested. Differences between patients and controls are indicated with asterisks (*P < 0.05) or with a dagger (^†P = 0.09). Brackets indicate SEM.

Fig. 3.

Exp. 3. Performance on two 16-item recognition memory tests for faces when accuracy for controls was at least as good for faces as it was for buildings and words in Exp. 2. Memory-impaired patients with damage limited to the hippocampus (H; white bars) performed as well as controls (CON; black bars). A patient with larger lesions of the MTL (gray bar) was impaired. Brackets indicate SEM.

Fig. 4.

Exp. 4. Performance on a recognition memory test for famous faces for a control group (CON; black bars) and for memory-impaired patients with damage limited to the hippocampus (H; white bars) or larger lesions of the MTL (gray bar). Participants studied 50 famous faces and then immediately took a recognition memory test involving the 50 previously studied faces and 50 new famous faces. (A) Both H and MTL patients were impaired. (B) Accuracy was examined separately according to whether the faces could be identified as famous. H patients were impaired for known famous faces but performed as well as controls for faces that they did not identify as famous. The MTL patient was impaired regardless whether he could identify the faces as famous. Asterisks indicate a significant difference between H patients and controls (*P < 0.05). Brackets indicate SEM.

Fig. 5.

Exp. 5. Performance on two eight-item recognition memory tests for inverted faces for a control group (CON; black bars) and for memory-impaired patients with damage limited to the hippocampus (H; white bars) or larger lesions of the MTL (gray bar). H and MTL patients were impaired relative to controls at discriminating old and new inverted faces. Asterisk indicates a significant difference between H patients and controls (*P < 0.05). Brackets indicate SEM.