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When recognition memory is independent of hippocampal function
Authors:Christine N. Smith  Annette Jeneson  Jennifer C. Frascino  C. Brock Kirwan  Ramona O. Hopkins  Larry R. Squire
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.The hippocampus and related medial temporal lobe (MTL) structures are essential for the formation of long-term declarative memory. Damage to these structures has traditionally been thought to result in a broad memory impairment that extends across all sensory modalities, across all domains of material (e.g., scenes, words, objects), and across different testing methods (e.g., recall and recognition) (13).An early hint that the impairment might not be so pervasive came from a study of recognition memory in a mixed group of memory-impaired patients (4). Three patients thought to have hippocampal lesions were impaired at word recognition but not at face recognition. Subsequently, recognition scores on the same test were reported for a larger group (n = 6, including the earlier three patients). Again, word recognition was poor, but face recognition was variable and not significantly impaired (P < 0.08) (5). Because of this marginal finding, and the finding that face recognition was unequivocally impaired at a retention delay of 24 h (5, 6), the possibility that face recognition might be special in some way was not noted. Face recognition also drew no comment when it was reported to be intact in a single patient (patient BE) (7).An early review of the literature suggested that the performance of hippocampal patients was good for face recognition but concluded that performance was also good for recognition memory more broadly (8). Similarly, an extensive study of hippocampal patient YR emphasized the relative sparing of recognition memory, including face memory, against a background of impaired recall (9). Other studies suggested that what was spared was recognition of nonverbal material (10) or single-item recognition, compared with associative recognition (11).Perhaps the first proposal that the capacity for face recognition itself deserved special attention came from the study of a patient with hippocampal lesions and spared face recognition memory but impaired recognition memory for words and buildings (12). Subsequently, three single-case studies and one group study (n = 3) also reported spared memory for faces after hippocampal lesions and impaired memory for other kinds of nonverbal material (e.g., buildings or scenes) (1316). The evidence for sparing of face recognition became even stronger when scores on the Recognition Memory Test [RMT, a standard memory test for faces and words (17)] were brought together for 10 patients with hippocampal lesions from earlier studies (18). The findings were unmistakable. Recognition memory was impaired for words but intact for faces. The authors suggested that hippocampal lesions might spare recognition memory for material that, like faces, was unfamiliar to patients before testing.In five experiments, we explored the conditions under which face recognition memory might be spared in patients with hippocampal lesions (H) or larger lesions of the MTL. We first examined scores on a standard test (the RMT). For four patients (three H patients and one MTL patient) neurohistological information was available to characterize the lesions. For six patients the lesions were characterized by quantitative neuroimaging (Table S1). Testing occurred both immediately after study and 24 h later (Exp. 1). Next, for the six patients still living (five H patients, one MTL patient), we assessed recognition memory for faces, buildings, and words across four retention intervals from immediate to 1 d (Exp. 2). We then tested face recognition memory again after matching the difficulty of the faces and buildings tests (Exp. 3). Next, we tested recognition memory for faces that were potentially familiar to participants before testing (i.e., famous faces from before 1970; Exp. 4). Finally, we tested recognition memory for upside-down faces (Exp. 5).
Keywords:amnesia   long-term memory
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