Both groups reported significant increases in their level of sadness (AD: t16=10.32, P<0.001; healthy comparisons: t16=12.88, P<0.001) immediately after watching the sad film clips, indicating that the sadness induction was effective (Figure 2). The 2 groups reported similar levels of sadness and negative affect. The groups did not differ significantly in their sadness VAS ratings and negative affect after the induction (F1,32=2.40; F1,32=3.42), after the memory test (F1,32=0.01; F1,32=0.88), or in the final rating (F1,32=0.86; F1,32=0.63).
After the memory test, the AD group reported significantly more positive affect than the healthy comparison group (F1,32=4.43, P<0.05). There was no significant between-group difference in positive affect after the induction (F1,32=1.42) or in the final rating (F1,32=0.31). Table 5 shows more detail about the emotion ratings.
In strong support of our hypothesis, the patients with AD reported feeling elevated levels of sadness that lasted for up to 30 minutes after the films, despite having little or no recollection of the content (Figure 3). The AD group’s mean change in sadness from baseline to immediately after the induction was 65.29; after the memory test, 35.88; and in the final rating, 28.53. Across all participants, the correlation between memory performance and sadness during the final rating was significant, but in a negative direction (r=−0.37, n=34, P<0.05). This paradoxical effect actually suggests that the less the patients remembered about the films, the longer their sadness lasted.
The dissociation between lingering feelings and impaired declarative memory was especially compelling in 4 patients with AD who could not recollect any details about the films. Despite their severe memory impairment, all 4 patients reported sustained feelings of sadness after the memory test, and 3 reported feeling sad even at the final rating 30 minutes post-induction (Figure 4).
We found no significant between-group differences in Inventory of Depression and Anxiety Symptoms scores (t16=1.16), sadness VAS at baseline (t16=0.23), or negative affect at baseline (t16=2.17). To explore further the influence of depressive symptoms on the experience and sustainability of sadness, we conducted a 2×2 (time × group) multivariate analysis of covariance. We used the last 2 emotion measures, “after memory test” and “final rating,” as dependent variables, because these measures reflected sustained feelings of sadness, and we used scores on the Inventory of Depression and Anxiety Symptoms as the covariate. The analysis was not significant (F2,30=0.99, P=0.38). These results suggest that individual differences in depressive symptoms in our participants were not significantly related to their sustained experience of sadness.
The AD group retained significantly less information about the happy films than did the healthy comparison group (t16=11.17, P<0.001) (Figure 1). Five patients with AD were unable to recall any factual details about the happy films. The AD group also performed significantly worse than the healthy comparison group on both verbal recognition (t16=4.91, P<0.001) and picture recognition (t16=3.17, P<0.01) (Table 4).
We found a significant increase in level of happiness in both the patients with AD (t16=3.41, P<0.01) and the healthy comparison participants (t16=5.51, P<0.001) immediately after they watched the film clips (Figure 5). The baseline happiness VAS ratings did not differ significantly between groups (t16=1.61).
There were no significant between-group differences in happiness ratings obtained after the induction (F1,32=0.12), after the memory test (F1,32=0.04), or in the final rating (F1,32=0.00). Moreover, the groups did not differ significantly in their negative or positive affect ratings obtained after the induction (negative: F1,31=0.68; positive: F1,31=2.26), after the memory test (F1,31=0.40; F1,31=0.39), or at the final rating (F1,31=0.90; F1,32=0.87). Table 6 lists more detailed information about the emotion ratings.
Similar to what we found with the sadness induction, 3 patients with AD had no recall at all for the happy films but continued to experience happiness beyond the memory test, and 2 of them showed elevations in happiness that persisted 30 minutes after the end of the films (Figure 6). This finding further illustrates the dissociation between impaired declarative memory and sustained feelings. We found no significant relationship between memory performance and ratings of happiness during the final rating (r=0.06, n=34).
We found that patients with AD reported feeling sustained states of happiness and sadness despite their impaired declarative memory for the events that had originally triggered the emotional state. Our findings are consistent with previous studies showing that individuals with AD have relatively preserved emotion (Blessing et al, 2006, 2012; Evans-Roberts and Turnbull, 2011). However, our study goes beyond assessing the implicit learning of emotional information and demonstrates that patients with AD are profoundly impacted emotionally by events that they cannot recall. In other words, their feelings persist long after the memories have vanished. Thus, patients with AD exhibit the same phenomenon of “feelings without memory” that we had observed in patients with hippocampal amnesia (Feinstein et al, 2010).
The patients with AD also showed another pattern similar to the patients with hippocampal amnesia: Those patients who had the worst memory for the sad films tended to experience the most prolonged states of sadness (Figures 3 and 4). This counterintuitive finding suggests that a free-floating state of negative emotion, untethered from the original emotion-inducing memory, might be particularly difficult to manage.
This difficulty may stem from the adaptive value of knowing the cause of our negative emotions, which in turn can help expedite our recovery from them. A free-floating state of emotion, especially a negative emotion, triggers a search process aimed at discovering the source of the emotional disturbance (Feinstein, 2013). Unfortunately, the amnesia in patients with AD prevents them from being able to make any conclusive discovery. Their inability to attribute the source of the aberrant emotional state draws further attention to it, in effect creating a positive feedback loop that hijacks the natural recovery process and ultimately leads to an abnormally prolonged state of emotion.
For example, near the end of the post-induction period in this study, a patient with AD who had no recollection for any of the sad films stated, “I feel like all my emotions and feelings are rushing in on me. It’s extremely confusing and I do not like that feeling.” The persistence of this patient’s intense negative emotion and her inability to conjure up a logical explanation for the cause of her feelings illustrate the bewilderment that a patient with AD may experience in the face of an apparently inexplicable feeling.
Other patients reported remembering that something sad had happened but could not recall details about the source of their sadness. One patient said, “They showed so much heartache. I don’t recall seeing joy, just pain and heartache”; again, she could not provide any details. Her reaction echoes research showing that patients with AD may have “source amnesia,” ie, they can recall information but not where, how, or under what circumstances they learned it (Dalla Barba et al, 1999).
Our findings support the idea that the neural systems underlying emotional processing and feeling may be relatively preserved in individuals with AD, especially during the early stages. Previous research has shown that amygdala volumes are positively associated with emotional memory (Adolphs et al, 1997; Cahill et al, 1995; Hamann et al, 1997; Mori et al, 1999). Thus, it is possible that our study patients with AD who sustained the induced emotion may have relatively preserved amygdala function. Understanding the neuroanatomic underpinnings of the ability to sustain an emotion deserves further research, and our laboratory is currently working on this topic.
Our study had several limitations. First, our sample size was only moderate. However, both our individual cases and group means demonstrated that patients with AD can experience feelings for an extended period of time despite impaired declarative memory for what caused the feelings.
Second, our data on feelings were derived from self-report. It could be argued that patients with AD might have difficulty comprehending the questions and identifying their feelings (Sturm and Levenson, 2011). However, several points argue against this as a major explanation of our findings. First, before accepting the patients with AD into the study, we carefully tested them with neuropsychological measures to ensure that they had adequate comprehension to perform the study procedures. Second, the AD group and the healthy comparison group reported similar intensities of induced sadness or happiness, and both groups reported a concomitant decrease in positive affect when their negative affect increased after the sadness induction (Figure 2B), suggesting that the patients were rating their feelings reliably and validly. Third, while watching the films, the patients displayed emotional behaviors, such as crying or laughing, that were consistent with the feelings that they later reported. Previous studies looking at emotional reactivity in patients with AD have also shown preserved facial responses to emotional film clips (Mograbi et al, 2012; Smith, 1995).
A final limitation of our study was that the happy films were not as effective as the sad films at inducing strong emotions. This pattern is in keeping with a common trend in the literature. Inducing happiness in the laboratory is challenging, and negative emotions are generally reported to be more salient than positive emotions (Gerrards-Hesse et al, 1994; Monteil and Francois, 1998). One possible explanation for the difficulty of inducing happiness in the laboratory is that participants tend to report high levels of happiness at baseline (Gerrards-Hesse et al, 1994; Monteil and Francois, 1998). This explanation is consistent with our findings.
Our study highlights the fact that actions toward patients with AD have consequences, even when the patients do not appear to remember the actions. In fact, actions may have a lasting impact on how the patients feel. Older adults in nursing homes and patients with AD can be victims of both verbal and physical mistreatment by staff or caregivers (Schiamberg et al, 2012; VandeWeerd et al, 2006, 2013). Such mistreatment may explain in part the increases in psychiatric symptoms and feelings of loneliness seen in people who have moved into a nursing home (Karakaya et al, 2009; Scocco et al, 2006).
Our findings suggest that even though patients with AD may not remember instances of maltreatment, they can still experience the negative emotions triggered by such events. The fact that these patients’ feelings can persist, even in the absence of memory, highlights the need to avoid causing negative feelings and to try to induce positive feelings with frequent visits and social interactions, exercise, music, dance, jokes, and serving patients their favorite foods. Thus, our findings should empower caregivers by showing them that their actions toward patients really do matter and can significantly influence a patient’s quality of life and subjective well-being.
The fact that forgotten events can continue to exert a profound influence on a patient’s emotional life should be applied to the standard of care in nursing homes and assisted living facilities, and implemented by all caregivers. Jade Angelica (2013) has proposed that caregivers should not try to make patients conform to our version of “reality” because such efforts can leave patients feeling upset and confused. Instead, caregivers should try to view reality from the patient’s perspective and approach the patient with empathy. By adopting an attitude of acceptance and giving patients constant reassurance and positive affirmation, caregivers can potentially induce prolonged states of positive emotion while minimizing negative emotion and instances of noncompliant and aggressive behavior. Similarly, because positive feelings can persist, caregivers should be encouraged to continue interventions such as social dancing (Palo-Bengtsson and Ekman, 2002) and therapeutic games (Cohen et al, 2009).
Despite the considerable amount of research aimed at developing disease-modifying pharmacotherapies for AD, no drug has succeeded at either preventing or substantially influencing the disease’s progression. Against this foreboding backdrop, we would like to suggest that more resources be devoted to the research and dissemination of caregiving techniques that could improve the well-being and minimize the suffering for the millions of individuals afflicted with AD (Angelica, 2013; Edvardsson et al, 2012; Thies et al, 2013). Such a paradigm shift will become even more imperative as the population continues to age and the number of patients with AD rises to epidemic proportions.
The authors thank Karen Peralta, Ganna Savranska, Samantha Korns, and Emily Eilers for help with data collection and management; Jade Angelica for valuable comments; the staff at the Benton Neuropsychology Laboratory and the Alzheimer’s Association for assisting with recruitment; Oliver Turnbull and Daniel Mograbi for their perceptive reviews; and Don Fowles for his insightful comment that became the catalyst for this line of inquiry.
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Keywords:© 2014 by Lippincott Williams & Wilkins.
amnesia; emotion; aging; declarative memory; emotional memory