Department of Clinical Neurosciences, Hyogo Institute for Aging Brain and Cognitive Disorders, Himeji, Japan
Department of Neurobiology and Behavior and Center for the Neurobiology of Learning and Memory, University of California, Irvine, USA
Correspondence: Dr Hiroaki Kazui, Department of Clinical Neurosciences, Hyogo Institute for Aging Brain and Cognitive Disorders, 520 Saisho-ko, Himeji, 670-0981, Japan. Tel.: +81 792 95 5511 ; fax: +81 792 95 8199; e-mail: kazui{at}hiabcd.go.jp
1 Long-term memory is differentiated into declarative memory and procedural
memory. Declarative memory is explicit and conscious and it consists of
information based on specific facts or data. Procedural memory is assessed by
performance of particular skills and is usually retained in amnesia.
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ABSTRACT |
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Aims To test our previous findings in a controlled experimental study.
Method Recall tests consisting of two short stories were administered to 34 patients with Alzheimer's disease and 10 normal subjects. The two stories were identical except for one passage in each story: one was emotionally charged (arousing story) and the other (neutral story) was not.
Results In both groups, the emotionally charged passage in the arousing story was remembered better than the counterpart in the neutral story. In addition, the extent of the memory improvement was similar in the subjects and in the controls.
Conclusions The results provide further evidence that emotional arousal enhances declarative memory in patients with Alzheimer's disease, and give a clue to the management of people with dementia.
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INTRODUCTION |
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METHOD |
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The subjects were 34 Japanese patients (27 women and 7 men) with probable Alzheimer's disease and 10 normal elderly control subjects matched for age, gender and educational attainment. The normal controls were seven women and three men recruited from the community, who had no neurological signs or significant medical antecedents. The Mini-Mental State Examination (MMSE; Folstein et al, 1975) was administered to all normal subjects. The patients with Alzheimer's disease were recruited from those who were admitted to our hospital for examination, according to the criteria below. All patients were examined by both neurologists and psychiatrists during a short-term hospital stay and given routine laboratory tests and standard neuropsychological examinations; in addition, an electroencephalogram, an MRI brain scan, and MR angiograms of the neck and head were obtained. The inclusion criteria were those of the National Institute of Neurological and Communicative Disorders and Stroke/Alzheimer's Disease and Related Disorders Association for probable Alzheimer's disease (McKhann et al, 1984). The exclusion criteria were: (1) any complication due to other neurological or physical illness; (2) any MRI evidence of focal brain lesions and of cerebral arterial occlusive lesions on MR angiography; and (3) severe cognitive, attentional, or behavioural disorders which would make memory tests difficult. The severities of dementia as rated by the Clinical Dementia Rating (CDR; Hughes et al, 1982) were 0.5 (minimal) for four patients, 1 (mild) for 25, 2 (moderate) for four, and 3 (severe) for the remaining one. The MMSE and Alzheimer's Disease Assessment Scale Cognitive sub-scale (ADAScog; Mohs et al, 1983) were administered to all Alzheimer's subjects. Table 1 summarises the demographic and cognitive characteristics of the subjects.
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The 34 Alzheimer's disease patients were divided into two groups: one group was read an arousing story, then, 2 weeks later, a neutral story (AD-AN); the other was read a neutral story, followed 2 weeks later by an arousing story (AD-NA). The groups were comparable in age and gender, educational attainments, MMSE scores, and ADAScog scores. The 10 normal elderly subjects (NC) were also divided into two similarly comparable groups (NC-AN and NC-NA) (except for ADAScog scores). Table 2 summarises the demographic and cognitive characteristics of subjects in the four groups.
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ASSESSMENT |
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Both types of story consisted of three phases. For the first four of the 11 photographs (phase 1), the narrations in the arousing story were identical to those in the neutral story. In this phase, both stories depicted a mother taking her son to visit his father at work. In the middle four photographs (phase 2), the narrations in the arousing story differed from those in the neutral story: phase 2 of the arousing story was emotionally charged and phase 2 of the neutral story was not. In phase 2 of the arousing story, the boy was badly hurt in an automobile accident, and surgeons struggled to save his life; while in phase 2 of the neutral story, the boy watched a disaster drill in the hospital. For the last three photographs (phase 3), the narrations in the arousing story were nearly identical to those in the neutral story: phase 3 of both stories depicted the mother leaving the hospital. The arousing and neutral stories are closely matched in content, complexity and style, and were confirmed to be matched in comprehensibility (Cahill & McGaugh, 1995).
The subjects were told to pay close attention to the photographs and the narrative and to remember the story. Immediately following the presentation of the story, they were asked to rate the emotional charge of the stories on a scale of 1-4 (1 indicating not emotional and 4 indicating highly emotional).
After rating the emotional charge of the stories, and 5 minutes after the end of the presentation of the photographs, the subjects were given an 11-item recall test. We did not use the standard methods of the recall test, because the Alzheimer's disease patients' amnesia was severe. Instead, we used a simplified version of the recall paradigm. As the photographs were presented one by one again in the same order, subjects were asked questions about the story line (one question per photograph). If they could answer a question perfectly, they scored 2 points; if they could not answer at all, they scored 0 points; if their answer was partially correct, they scored 1 point. Thus, the maximum scores of phases 1, 2 and 3 were 8, 8 and 6 points. Recall scores were expressed as a percentage of the maximum of each phase, because of the different numbers of questions given for each phase.
The second part of the experiment was carried out 2 weeks later. On this occasion, those groups who had been read the arousing story 2 weeks previously were now read the neutral story, and those who had been read the neutral story 2 weeks previously were now read the arousing story. The scores in the AD-AN and AD-NA groups were evaluated together as scores of the Alzheimer's disease subjects, and the scores in the NC-AN and NC-NA groups were evaluated together as scores of the normal controls.
Statistical analysis
The rating of the emotional charge of the stories was analysed by using
two-way analysis of variance (ANOVA) for repeated measures with one
between-factor (group) and one within-factor (story). The recall scores across
the three phases on the assessment of emotionally influenced memory was
analysed by using three-way ANOVA for repeated measures, with one
between-factor (group) and two within-factors (story and phase). To
specifically elucidate the effect of emotional arousal on memory we carried
out two-way ANOVA for repeated measures with two within-factor (story and
phase) and a post hoc Tukey honestly significant difference test. The
statistically significant level was set at P <0.05.
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RESULTS |
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Emotionally influenced memory test
The results of the recall memory test for the three phases of the arousing
and the neutral stories for the Alzheimer's patients and the normal controls
are illustrated in Fig. 2. The
three-way ANOVA revealed a significant group effect (F(1,42)=94.0,
P < 0.0001), a significant story effect (F(1,42)=12.3,
P < 0.005), a significant phase effect (F(2,84)=6.88,
P < 0.005), and a significant story x phase interaction
(F(2,84)=30.1, P < 0.001). But the group x story
interaction (F(1,42)=4.02, P=0.052), group x phase
interaction (F(2,84)=30.1, P=0.21), and group x story
x phase interaction (F(2,84) =0.48, P=0.62) were not
significant.
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The two-way ANOVA for the Alzheimer's group revealed a significant story effect (F(1,34)=24.9, P < 0.001), a significant phase effect (F(2,68)=14.8, P < 0.001), and a significant story x phase interaction (F(2,68)=37.5, P < 0.001). The post hoc test showed that the recall scores in phase 2 were significantly worse for the neutral story than for the arousing story (P < 0.001), while the recall scores in phases 1 and 3 of the two stories were comparable. The analysis for the NC group revealed a significant story x phase interaction (F(2,18)=12.0, P < 0.001), but no significant story effect (F(1,9)=3.25, P=0.10) or phase effect (F(2,18)=1.8, P= 0.25). The post hoc analysis showed that the recall scores in phase 2 were significantly worse for the neutral story than for the arousing story (P < 0.005), while the recall scores in phases 1 and 3 for the two stories were comparable.
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DISCUSSION |
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Emotionally influenced memory in Alzheimer's disease
In the present study, the rating of the emotional charge of the arousing
story was significantly higher than that of the neutral story, in both the
Alzheimer's patients and the normal subjects, reconfirming that both groups
were similarly more emotionally charged by the arousing story than by the
neutral story. The Alzheimer's disease patients recalled less about the
stories than did the normal subjects, for both stories. A phase-by-phase
comparison of the results in each group showed that the arousing story was
better recalled than the neutral story only in phase 2, in which the emotional
impact in the arousing story was greater than that in the neutral one. These
results strongly indicate that the enhancing effect of emotional arousal on
declarative memory is preserved in patients with Alzheimer's disease, although
the memory function itself in such patients was poorer than in normal
subjects.
Magnitude of enhancement
From a neuroanatomical viewpoint, the amygdala is considered to play a
crucial role in emotionally influenced memory (Cahill et al,
1996,
1998;
Hamann et al, 1999).
Adolph et al (1997)
demonstrated the failure of the enhancing effect of emotional arousal on
memory in patients with bilateral damage to the amygdala, using the same
emotional memory paradigm that was used in the current study. In our previous
study we reported that emotional remote memory about a terrible earthquake was
significantly more closely correlated with the volume of the amygdala than
with the volume of the hippocampus in Alzheimer's patients, indicating that
the impairment of the enhancing effect of emotional arousal on memory in these
patients is related to the degree of damage to the amygdala
(Mori et al, 1999).
That study also indicated that in some Alzheimer's patients, arousal material
failed to enhance memory. However, in the present study, the magnitude of the
enhancement of memory in Alzheimer's patients by emotional material was as
good as that in normal subjects.
One possible reason for this discrepancy might be the difference in the severity of dementia in the target subjects. In the patients in the present study, dementias were milder than those in our previous study, as rated by the CDR. The volume of the amygdala decreased and the neuropathological changes in that region increased with increasing CDR score (Jack et al, 1997; Haroutunian et al, 1998). Because more of the amygdala was probably preserved in the patients in this study than in those in our previous study, those in the present study might have had a greater memory for emotional material.
Another possible reason for this discrepancy might be the easiness of the current recall test. The recall test in the present paradigm was made easier to enable us to assess the memory function fairly and to avoid the floor effect in Alzheimer's disease. Consequently, the recall test might have become too easy for the normal subjects, and a ceiling effect might have occurred in phase 2 for the arousing story in the normal subjects, which would have artificially decreased the degree to which the arousing story enhanced their memory.
Clinical implications of emotionally influenced memory
The finding that emotional arousal enhanced memory in Alzheimer's disease
has implications for the management of people with dementia. It directly
suggests that they should be treated gently, to avoid eliciting strong
negative feelings. Although Alzheimer's patients forget less emotional events,
they have a better memory for emotionally negative events, and this might
damage the caregiverpatient relationship, for example. Although the
emotional arousal used in the present study was negative in nature, both
positive and negative emotional arousal have similar memory-enhancing effects
(Hamann et al,
1997b). In consideration of our finding, together with
this evidence of Hamann et al, it is suggested that the instructions
and guidance given to Alzheimer's disease to patients may be easier to
remember if emotionally arousing actions, devices and so on are used.
The present finding also implies a potentially useful strategy for memory rehabilitation. Furthermore, the fact that emotional arousal enhances memory raises the possibility of enhancing memory without emotional arousal, by using agents such as the ß-adrenergic receptor agonist and the corticosterone receptor agonist, which involve the final emotionmemory pathway (Cahill et al, 1998). Clearly, more research is needed to determine the association between emotion and memory and to develop a useful strategy for memory enhancement.
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Clinical Implications and Limitations |
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LIMITATIONS
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Received for publication November 23, 1999. Revision received March 27, 2000. Accepted for publication April 4, 2000.