Retrograde Amnesia

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Loss of premorbid memory (retrograde amnesia) following damage to the medial temporal lobe has been documented extensively, and has also been discussed in the context of the distinction between episodic and semantic memory. However, a difficulty arises in the case of past memory, especially remote autobiographical memory, because it is not easy to agree as to when an individual is engaged in episodic retrieval of specific events and when an individual is drawing on a well-rehearsed base of semantic knowledge. This point was developed in some detail by Cermak (1984). Consequently, caution is merited when trying to interpret the facts of retrograde amnesia in terms of episodic and semantic memory. Regardless of uncertainties about definition, it remains important to assess the quantitative and qualitative features of remote memory for facts and events in amnesic patients. Is remote memory intact? Or is there some aspect of remote remembering that is lost after medial temporal lobe lesions or restricted hippocampal lesions? The question of interest, then, is how the capacity of amnesic patients to recollect past facts and events compares with the capacity of intact individuals and how this capacity relates to neuroanatomy.

With respect to the recall of facts, patients with histologically-confirmed lesions limited to the hippocampal formation (patients L.M. and W.H.; Rempel-Clower et al., 1996) were found to be impaired at recalling news events and other factual information that occurred a decade or more before the onset of their amnesia (Beatty et al., 1987, 1988; Rempel-Clower et al., 1996; Squire et al., 1989). Information about more remote facts was intact. It seems unlikely that normal individuals could consistently evoke the learning episode when recollecting 10 year-old facts; and if individuals do not remember the learning episode, then such recollections must be based on semantic memory. Accordingly, these findings suggest that the hippocampal formation is important for retrieval of recently acquired semantic memory (for additional evidence, see Schmidtke & Vollmer, 1997; Verfaellie et al., 1995).

Larger lesions of the medial temporal lobe also spare remote memory for factual knowledge. E.P. became amnesic in 1992 at the age of 70, after an episode of herpes simplex encephalitis. He has extensive, virtually complete bilateral damage to the hippocampus, amygdala, entorhinal cortex and perirhinal cortex, as well as damage to the anterior parahip-pocampal cortex and anterior fusiform gyrus (Stefanacci et al., 2000). E.P. grew up in the Hayward-Castro Valley area of California during the 1930s and 1940s, moved away at the age of 28, and has returned only occasionally. E.P. was age-matched to five controls who attended his high school, lived in the area about as long as he did, and also moved away at about the age that he did. All six individuals were given four tests of topographical memory to assess their spatial knowledge of the region where they grew up (Teng & Squire, 1999). They were asked to describe how they would navigate from their homes to different locations in the area (familiar navigation), between different locations in the area (novel navigation), and between these same locations when a main street was blocked off (alternative routes). They were also asked to imagine themselves in particular locations and facing particular directions and then to point towards specific landmarks (pointing to landmarks). E.P. performed well on all four tests (Figure 4.4). In contrast to E.P.'s superb navigational knowledge about where he grew up, he has no knowledge of his current neighborhood, where he has lived since 1993 (after he became amnesic).

These findings indicate that factual (semantic) knowledge about the remote past is independent of medial temporal lobe structures. It is also interesting that the cognitive abilities that permit E.P. to reconstruct the layout of the neighborhood that he lived in 50 years ago does not permit him to acquire similar knowledge about his current neighborhood. The ability to acquire this new knowledge depends on the medial temporal lobe.

A different amnesic patient (K.C.) was able, like E.P., to answer questions about the spatial layout of the neighborhood in which he grew up, and succeeded altogether at six

Figure 4.4 Performance on four tasks of topographical memory for patient E.P. (open circles) and five control subjects (closed circles). (A) Percentage correct score on three navigation tasks within the neighborhood where participants grew up. The tasks required recalling either familiar routes, novel routes, or alternative routes (when the most direct route was blocked). (B) Median error in degrees on a task in which participants pointed to particular locations while imagining themselves oriented at other locations. (C) Percentage correct score on a navigation task of participants' current neighborhood. Adapted from Teng & Squire (1999)

Figure 4.4 Performance on four tasks of topographical memory for patient E.P. (open circles) and five control subjects (closed circles). (A) Percentage correct score on three navigation tasks within the neighborhood where participants grew up. The tasks required recalling either familiar routes, novel routes, or alternative routes (when the most direct route was blocked). (B) Median error in degrees on a task in which participants pointed to particular locations while imagining themselves oriented at other locations. (C) Percentage correct score on a navigation task of participants' current neighborhood. Adapted from Teng & Squire (1999)

tests of remote spatial memory (Rosenbaum et al., 2000). However, K.C. was impaired at recognizing pictures of houses and other landmarks in his neighborhood and at locating cities on maps of Canada and the province of Ontario where he lived. This pattern of performance is difficult to interpret in the context of medial temporal lobe function because K.C.'s amnesia is the result of a closed-head injury. Magnetic resonance imaging indicates that the injury damaged not just the left medial temporal lobe and a small portion of the right medial temporal lobe but also did substantial damage to the left frontal, left parietal, left retrosplenial and left occipital corticies. A smaller lesion is also present in the right parietal cortex. Accordingly, it is unclear what aspects of K.C.'s impaired performance are attributable to medial temporal lobe pathology. In summary, patients with histologically-confirmed lesions limited to the hippocampal formation (L.M. and W.H.), and a patient with a radiologically-confirmed lesion limited largely to the medial temporal lobe (E.P.), have good access to factual knowledge from their early life.

The ability of amnesic patients to retrieve autobiographical (episodic) memories from their past has also been studied at some length. It has been useful to ask whether amnesic patients can produce autobiographical recollections and to consider how their recollections compare to those produced by normal individuals. The matter is of interest because of early suggestions that amnesic patients may not be capable of true autobiographical remembering (Cermak, 1984; Kinsbourne & Wood, 1975), and because patient K.C. reportedly cannot produce specific event-based recollections (Tulving et al., 1988). More recently, this idea has been applied to medial temporal lobe amnesia, and it has been suggested that the remote autobiographical memories produced by patients with medial temporal lobe damage lack the detail found in the recollections of normal individuals (Nadel & Moscovitch, 1997; Nadel et al., 2000).

Figure 4.5 (A) Total score for patient R.B. and six controls (CON) on 10 autobiographical recollections when each recollection was scored on a 0-3 scale for content. From Zola-Morgan et al., 1986). (B) Total scores for patients L.M. and W.H. and five controls (CON) on five autobiographical recollections from childhood and adolescence when each recollection was scored on a 0-3 scale for content. From MacKinnon & Squire (1989)

Figure 4.5 (A) Total score for patient R.B. and six controls (CON) on 10 autobiographical recollections when each recollection was scored on a 0-3 scale for content. From Zola-Morgan et al., 1986). (B) Total scores for patients L.M. and W.H. and five controls (CON) on five autobiographical recollections from childhood and adolescence when each recollection was scored on a 0-3 scale for content. From MacKinnon & Squire (1989)

These issues have been investigated in patients whose lesions were subsequently identified in the course of a detailed neurohistological examination. Patient R.B. became amnesic in 1978, at the age of 52, as the result of an ischemic event that occurred as a complication of open heart surgery (Zola-Morgan et al., 1986). After his death in 1983, a circumscribed bilateral lesion was found in the CA1 region of the hippocampus. Minor pathology was found elsewhere (left globus pallidus, right postcentral gyrus, left internal capsule, patchy loss of cerebellar Purkinje cells), but the only damage that could be reasonably associated with the memory impairment was in the hippocampus. R.B. was given the Crovitz wordprobe test, which involves presenting single words (e.g. "bird", "ticket", "window") as cues and asking for an autobiographical recollection of a specific event from any period in the past that involves the cue word (Crovitz & Schiffman, 1974). R.B. produced well-formed episodic memories, and his score was as good as the average score obtained by six controls (Figure 5A). Each of 10 recollections was scored on a 0-3 scale, and a score of 3 was assigned when the recollection involved a specific, detailed memory of an episode. Thus, despite a lesion that would be expected to markedly disrupt the function of the hippocampus, R.B. could recollect autobiographical episodes as well as normal individuals.

Two other patients, L.M. and W.H., became amnesic at the age of 54 and 63, respectively. They were subsequently found to have bilateral lesions involving all the cell fields of the hippocampus (Rempel-Clower et al., 1996). There was also extensive loss of cells in the dentate gyrus and some cell loss in the entorhinal cortex. In addition, W.H. had extensive, patchy cell loss in the subiculum. The only damage detected outside the hippocampal formation was in the medial septum, right lateral occipitotemporal cortex and left medial temporal sulcus (patient L.M.) and in the pons and striatum (patient W.H.). Both patients also had patchy loss of cerebellar Purkinje cells, as frequently seen in cases of ischemia and anoxia.

1980s 1970s 1960s 1950s Before

1950

Figure 4.6 Time periods from which two patients (L.M. and W.H.) and five controls drew autobiographical memories in response to 75 single-word cues. L.M. and W.H. became amnesic in 1984 and 1986, respectively. From Rempel-Clower et al. (1996)

1980s 1970s 1960s 1950s Before

1950

Figure 4.6 Time periods from which two patients (L.M. and W.H.) and five controls drew autobiographical memories in response to 75 single-word cues. L.M. and W.H. became amnesic in 1984 and 1986, respectively. From Rempel-Clower et al. (1996)

These two patients were given a number of tests of autobiographical remembering (MacKinnon & Squire, 1989). Although both patients had difficulty producing recollections from their recent past, when the questions concerned their childhood and adolescence, they performed well. For example, one test asked structured questions about common events likely to have been experienced by most persons, e.g. "Tell me as much as you can about: your most embarrassing moment in high school; the day you first got your driver's license; the day you learned to ride a bike". Although only five questions were asked of each participant, L.M., W.H. and the controls performed similarly. Figure 4.5B shows their performance when each recollection was scored on a 0-3 scale.

In another test, 75 single-word cues were given (Crovitz & Schiffman, 1974), and participants attempted to recollect a specific episode from their lives that involved each word. Control subjects, like typical middle-aged individuals (McCormick, 1979), drew their memories predominantly from the recent past and from the remote past, and less often from the middle of their lives (Figure 4.6). L.M. and W.H. differed strikingly from the controls with respect to the temporal distribution of their recollections. Specifically, they drew most of their recollections from before 1950 and produced very few recollections from the period after 1960. In 1960, L.M. was 30 years old, and W.H. was 37 years old. In summary, these findings for L.M. and W.H. suggest that autobiographical recall of remote episodes is spared in the presence of moderately severe amnesia and bilateral damage to the hippocampal formation.

Although these findings are consistent with the idea that remote episodic remembering is intact after damage to the hippocampal formation, it remains possible that more sensitive tests or more sensitive scoring methods will reveal some abnormality. The importance of these issues was underscored recently by a report in which five memory-impaired patients attempted to produce two autobiographical recollections from each of five periods of life (Moscovitch et al., 2000). The recollections were found to be abnormal when they were scored for the total number of details that were recounted as part of each recollection. These findings are not relevant in any clear way to the facts of medial temporal lobe amnesia. The five patients included patient K.C., a basal forebrain patient, a diencephalic patient, an Alzheimer's disease patient, and a post-encephalitic patient. Unfortunately, no other anatomical information was provided. Nevertheless, the study raises an important methodological point about the assessment of autobiographical recollections, namely, that scoring the number of details may provide a better measure of remote memory capacity than a simple 0-3 scale.

To consider this issue further, two amnesic patients (A.B. and L.J.) were given 24 singleword cues and asked to recollect a specific episode from their first one-third of life before the onset of their amnesia (Bayley & Squire, 2001). L.J., aged 60 at the time of the test, has a radiologically confirmed bilateral lesion confined to the hippocampal region (Reed & Squire, 1998). A.B., aged 59 at test, is presumed to have hippocampal damage because of his etiology (cardiac arrest), but this cannot be confirmed because he is ineligible for magnetic resonance imaging. Overall, the two patients provided well-formed episodic memories (score = 3.0 on a 0-3 scale) in response to 83.4% of the cue words (for controls, 94.8% of the cue words). The number of unique details per 3.0 point memory was 29.1 for L.J. and 29.9 for A.B. (control mean = 27.8, range = 21.1-35.0). In addition, the amnesic patients tended to repeat details during the testing session, presumably due to their anterograde amnesia (patients = 4.0 repeats; controls = 0.9 repeats). These results suggest, in keeping with what has been found with less thorough scoring methods, that the hippocampal formation is not required to produce detailed episodic memories from early life.

Continuing study of patient E.P. indicates that he also has considerable capacity for detailed autobiographical remembering from early life (Bayley & Squire, 2001; Reed & Squire, 1998). Thus, E.P. provided well-formed memories (score = 3.0) for 18 of 24 cue words (75%), and provided 22.7 unique details for each of these memories (Bayley & Squire, 2001). Because E.P.'s lesion extends laterally beyond the medial temporal lobe to involve the fusiform gyrus, it is difficult to know whether his slightly reduced performance is a consequence of medial temporal lobe damage. In any case, E.P. is capable of much more autobiographical remembering than patient K.C. (Tulving et al., 1988) and also much more than patient G.T., who has large temporal lobe lesions that involve the full lateral extent of the anterotemporal cortex (Reed & Squire, 1998).

It is also of interest that E.P. has mildly impoverished knowledge about living and nonliving things (Stefanacci et al., 2000; their Figure 11). For example, when asked to point to a drawing of a seal among seven other drawings of animals that live in the water, E.P. pointed to a seahorse. Overall on this test, he pointed correctly to 43 out of 48 items (control range = 47-48). On another test, E.P. performed just below the control range when asked eight yes/no questions about each of 24 different items. For example, he answered affirmatively when asked if a rhinoceros has antlers. Overall on this test, he was correct on all eight questions for six of the 24 items (control range = 8-18), and provided 162 out of 192 correct answers (control range = 162-181). Thus, E.P.'s autobiographical remembering occurs in the context of a mild impairment for some aspects of semantic knowledge (the names of objects and their properties). There is no suggestion in the data available to date that E.P.'s temporal lobe damage has affected his episodic memory more than his semantic memory.

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