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Journal of Alzheimer’s Disease xx (20xx) x–xx DOI 10.3233/JAD-140351 IOS Press

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Ecological Assessment of Emotional Enhancement of Memory in Progressive Nonfluent Aphasia and Alzheimer’s Disease

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Fiona Kumfora,b,c,∗ , John R. Hodgesa,b,c and Olivier Pigueta,b,c

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a Neuroscience

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b School

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Handling Associate Editor: Ricardo Allegri

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Research Australia, Sydney, Australia of Medical Sciences, The University of New South Wales, Sydney, Australia c ARC Centre of Excellence in Cognition and its Disorders, The University of New South Wales, Sydney, Australia

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Accepted 21 March 2014

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Keywords: Carer, depression, emotion, episodic memory, frontotemporal dementia, hippocampus, insula, stress

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INTRODUCTION

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Abstract. Background: Events which are imbued with emotion are typically remembered vividly and with more confidence than similar non-emotional events. The extent that emotional enhancement of memory is compromised in neurodegenerative disorders is unclear, despite differential effects of dementia on emotion processing ability. Objective: To examine emotional enhancement of memory using an ecologically valid task in progressive nonfluent aphasia (PNFA), an expressive language subtype of frontotemporal dementia, in comparison to Alzheimer’s disease (AD) and matchedcontrols. Methods: Twenty-five dementia patients (13 PNFA, 12 AD) and 10 controls viewed either an emotionally arousing or a closely matched non-emotional story. Multiple-choice recognition memory was tested after a 1-hour delay. The alternate story was presented two weeks later. Results: PNFA showed a similar level of memory for the emotional and neutral story, whereas both controls and AD remembered significantly more details from the emotional than the neutral story. Correlation analyses indicated that in PNFA, emotional story memory correlated with reduced emotion recognition, whereas in AD, neutral story memory correlated with visual recall memory performance only. Furthermore, in PNFA, reduced emotional memory enhancement was associated with increased carer stress and depression. Conclusion: Emotional memory enhancement is absent in PNFA, whereas emotion facilitates memory for real-life events in AD. Disrupted emotional memory enhancement in PNFA is associated with reduced emotion recognition ability, suggesting that widespread emotion processing dysfunction is present in this disease. Crucially, loss of emotional enhancement influences carer wellbeing, which represents an important avenue for future studies to examine.

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Everyday events are infused with emotion. The day of your wedding, the birth of your child, or a car accident represent significant life events that are typically ∗ Correspondence

to: Dr. Fiona Kumfor, Neuroscience Research Australia, PO Box 1165, Randwick, NSW, Australia. Tel.: +61 2 9399 1025; Fax: +61 2 9399 1047; E-mail: [email protected].

remembered easily and in great detail. Importantly, the emotional tone of such events appears to be crucial for their encoding and vivid recollection, accompanied by high degrees of confidence. This phenomenon—the emotional enhancement of memory effect—is proposed to depend on interactions between the frontal and temporal lobes [1–3]. The extent that emotional enhancement of memory is compromised in clinical populations has gained increasing interest, with

ISSN 1387-2877/14/$27.50 © 2014 – IOS Press and the authors. All rights reserved

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syndromes suggests that variables such as how realistic the event is and the degree patients engage in the event, influences the extent to which memory is enhanced. For example, emotional enhancement of memory has been demonstrated in patients with AD who experienced a severe earthquake [7], although emotional enhancement for word lists and sentences [9] and verbal descriptions of emotional events [26], appears to be absent. It is, therefore, important to examine emotional enhancement of memory for events that closely reflect the type of events these individuals may experience in day-to-day life. Examining emotional enhancement of memory using a naturalistic task is also important in order to gain insight into how socioemotional deficits may contribute to stress and burden of carers of these patients. Stress tends to be greater in carers of frontotemporal dementia than in carers of AD patients [27, 28]. Changes in cognition contribute significantly to carer burden, with memory and emotion processing deficits associated with increased burden regardless of dementia type [29]. Whether deficits in emotion processing and emotional enhancement of memory are associated with increased carer stress and burden in the PNFA subtype of frontotemporal dementia, however, is unclear. The first aim of this study was to examine emotional enhancement of memory in PNFA using an ecologically valid task and compare their performance to that of patients with AD, who show episodic memory deficits in the context of relatively preserved emotion processing [12, 30–32]. We hypothesized that PNFA patients would show attenuation of the emotional enhancement of memory effect, given their reported deficits in emotion processing, whereas we predicted emotional enhancement of memory would be preserved in AD, despite an overall reduction in episodic memory ability. The second aim of this study was to examine the relationship between emotional enhancement of memory, neuropsychological test performance, and caregiver variables to (i) identify the neurocognitive mechanisms that contribute to emotional memory in PNFA and AD, and (ii) examine the relationship between emotional enhancement of memory and carer burden and wellbeing.

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evidence suggesting that patients with lesions to the amygdala [4] and individuals with schizophrenia [5] show an attenuated memory advantage for emotional information. Whether emotional memory is compromised in patients with dementia, however, is less clear. To date, research has focused primarily on patients with Alzheimer’s disease (AD) and has reported inconsistent findings, with the emotional enhancement effect found to be intact in some studies [6–8], but not others [9]. Whether emotional enhancement of memory is affected in frontotemporal dementia, has been investigated very little to date [10], despite increasing evidence of a significant emotion disturbance in these patients [11, 12]. Progressive nonfluent aphasia (PNFA) is one of the two language subtypes of frontotemporal dementia. These patients present with relatively circumscribed expressive language deficits, with speech production typically effortful and labored [13]. These deficits occur in the context of well-preserved word comprehension [13, 14] and memory for non-verbal stimuli [15]. Neuroanatomically, pathological changes are observed in the perisylvian region, the anterior insula, and posterior Broca’s area, and may extend into the inferior and middle frontal gyri [16–18]. Importantly, these brain regions play a central role in emotion processing. For example, the anterior insula is involved in emotion recognition and self-awareness (e.g., [19, 20]), as well as autonomic arousal and fear conditioning [21], while the inferior frontal gyrus is implicated in empathy [22]. Thus, the progressive neurodegeneration seen in PNFA is likely to result in impairment of aspects of emotion processing and may also interrupt emotional enhancement of memory. Because of the chief symptomatology and complaints, research in PNFA has focused predominantly on the characterization of the language deficits experienced by these patients. Recently, however, emotion processing deficits have been reported, with PNFA patients showing reduced ability to recognize emotions from facial expressions [23, 24] and prosody [25]. Only one study has examined emotional enhancement of memory in PNFA to date, indicating that the enhancement effect is absent in these patients [10], in line with their deficits in emotion recognition. In addition, the results suggested that emotional enhancement of memory was associated with integrity of the right inferior frontal gyrus [10]. Crucially, however, this study used a simple visual recognition paradigm to assess emotional enhancement of memory. As such, the impact of emotion on memory for everyday events in these patients remains unclear. Research in other dementia

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MATERIALS AND METHODS

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Participants

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Thirteen PNFA and 12 AD patients were compared with 10 healthy age- and education-matched controls. Participants were recruited from FRONTIER,

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Background demographics and neuropsychological assessment

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Emotional memory assessment

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The Functional Rating Scale [35] was used to measure disease severity in the patient groups. All participants were assessed on neuropsychological measures of attention (Digit Span Forwards, maximum span [36]; Trail Making Test [37]), episodic memory (Doors Memory Test, Part A [38], Rey Complex Figure (RCF) copy and 3-minute delay [39]), language (naming and comprehension subtests of the Sydney Language Battery [40]) and emotion recognition (Ekman 60 [41]).

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an emotionally neutral event, which has been described previously in detail elsewhere [42–44]. In brief, participants were shown 11 visual slides using PowerPoint. On presentation of each slide, a short sentence was heard aloud in a neutral tone, which narrated the two events. While the images were identical for the two stories, the narration in the middle section (Phase 2; Slides 5–8) differed between the two story versions. In the emotional story version, a young boy is hit by a car and critically injured, whereas in the neutral story version, the young boy passes a minor car accident on his way to visit his father at work. Phase 1 (Slides 1–4) and Phase 3 (Slides 9–11) were essentially identical across the two story versions. Participants were randomly assigned to view either the neutral or emotional story first, and approximately 2-weeks later were tested on the alternate story version. During encoding, participants were instructed to pay close attention to the pictures and the story, but were not informed that their memory for the story would be tested later. Immediately following the presentation of the story, participants’ were asked to rate the story for understanding (/10) and emotionality (/10). After a 1-hour delay, filled with unrelated neuropsychological tests, episodic memory for the story was assessed using a detailed, well-established multiple-choice questionnaire, 76 questions in total. Between 5 and 9 questions were asked per slide.

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the frontotemporal dementia research clinic in Sydney, Australia. All patients were diagnosed according to current consensus criteria [13, 33]. Patients with PNFA typically presented with difficulties in speech output, manifesting as a marked distortion or slowing of speech with agrammatism and/or apraxia of speech. Furthermore, 12 of the 13 PNFA patients underwent PET scanning with Pittsburgh Compound B (PiB), an in vivo marker of underlying amyloid-␤ pathology indicative of AD pathology [14]. Eleven of the 12 cases returned a negative result, providing further support for a diagnosis of PNFA in these cases. The single positive case was reviewed by an experienced behavioral neurologist (JRH), who confirmed the PNFA diagnosis based on current clinical diagnostic criteria (e.g., intact sentence repetition), despite the positive PiB-PET result [13]. Patients with AD presented with episodic memory deficits including learning and retrieval of information, together with mild deficits in executive functioning and/or visuospatial deficits and naming. Control participants were recruited from local community clubs. For all participants, exclusion criteria included: history of psychiatric or neurological conditions including history of traumatic brain injury or stroke, use of centrally-acting medication, and limited proficiency in English. In addition, all controls were required to score >88/100 on the Addenbrooke’s Cognitive Examination-Revised, which is a general screening measure of cognition [34]. All participants or their Person Responsible provided informed consent according to the Declaration of Helsinki. The South Eastern Sydney Local Health District and the University of New South Wales ethics committees approved the study.

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We used a well-validated story paradigm to assess memory for an ecologically valid emotional event and

Carer burden and wellbeing The Zarit Burden Interview was administered to evaluate the impact of the disease on carer quality of life, psychological suffering, and family and social relationships [45]. Carers also completed the Depression, Anxiety and Stress Scale [46], a self-report measure of psychological wellbeing. Statistical analyses Data were analyzed using IBM Statistics SPSS Version 22. Kolmogorov-Smirnov tests were run to check suitability of variables for parametric analysis. Differences in performance between groups on the demographic and neuropsychological variables were investigated using univariate analyses of variance (ANOVA), or chi-square for categorical variables. Subjective ratings of understanding and emotionality of the two stories were investigated using repeated measures ANOVA with Story Version (Neutral, Emotional) as the within subjects variable, and Diagnosis (PNFA, AD, controls) as the between subjects

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variable. For the emotional memory task analyses, memory performance on each story was first divided into three phases (Phase 1: Slides 1–4; Phase 2: Slides 5–8; Phase 3: Slides 9–11) and total percent correct scores were calculated for each phase. Then, a repeated measures ANOVA was conducted with Story Version (Neutral, Emotional) and Phase (1, 2, 3) as the within subjects variables and Diagnosis (PNFA, AD, controls) as the between subjects variable. Following the initial analyses, post hoc analyses were conducted using Sidak correction for multiple comparisons to investigate main and interaction effects. Finally, Pearson one-tailed correlations, corrected for multiple comparisons at p < 0.01, were conducted to examine the relationship between performance on the emotional memory task, neuropsychological and carer variables in PNFA and AD patients. RESULTS

Neuropsychological assessment revealed profiles broadly consistent with the clinical profile of each dementia syndrome, shown in Table 2. In brief, PNFA performed below controls on a verbal naming task, reflecting their impaired speech production, and mild deficits in visuomotor processing speed (Trails A), although visuoconstruction ability (RCF copy) was intact. Importantly, consistent with prior studies, PNFA showed impaired facial emotion recognition (Ekman 60) compared to controls. In contrast, the AD group showed impaired performance on a visual recognition memory task (Doors A) and a visual recall memory task (RCF 3-minute delay) compared to controls and PNFA patients. They also showed mild impairments in language comprehension, in line with the mild semantic deficits reported in this group, while visuoconstruction ability (RCF Copy) and emotion recognition (Ekman 60) were comparatively preserved.

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Subjective ratings of understanding and emotionality No significant difference in subjective ratings of understanding was observed between stories (F(1,32) = 2.554, p > 0.05) or across diagnosis groups

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All groups were well matched for age, sex and education and patient groups were matched for disease duration (Table 1).

Table 1 Demographics of the study sample

Demographics Gender (M:F) Age (years) Education (years) Disease duration (months) FRS (Rasch Score)

PNFA n = 13

AD n = 12

Controls n = 10

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p

5:8 64.5 ± 9.4 13.2 ± 2.8 35.8 ± 16.1 2.6 ± 1.6

9:3 68.6 ± 7.8 11.5 ± 3.1 64.0 ± 55.2 1.6 ± 1.4

6:4 71.4 ± 5.5 14.4 ± 3.0 – –

3.45# 2.25 2.71 3.12 2.20

n.s. n.s. n.s. n.s. n.s.

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Values are mean ± standard deviation. n.s. p > 0.05. # Chi-squared value. FRS, Functional Rating Scale. Higher scores denote higher functioning. FRS scores missing for 1 PNFA and 1 AD patient. Table 2 Neuropsychological assessment of the study sample

Cognitive Test ACE-R (100) Digits-F Digits-B Naming (30) Comprehension (30) Doors A (12) RCF copy RCF 3-min delay Trails A (s) Trails B (s) Ekman 60 (60)

PNFA

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95.7 ± 3.6 7.6 ± 1.2 5.6 ± 1.2 26.1 ± 2.6 29.6 ± 0.5 10.8 ± 1.0 31.2 ± 3.2 18.2 ± 6.4 34.5 ± 10.1 84.4 ± 29.1 50.3 ± 5.0

18.94 12.51 14.16 3.49 13.76 14.51 1.00 11.41 4.62 3.24 8.17

** ** ** * ** ** n.s. ** * n.s. **

Post hoc test Patients < Con Patients < Con Patients < Con PNFA < Con AD < Con; PNFA AD < Con; PNFA – AD < Con; PNFA PNFA < Con – PNFA < Con

Values are Mean ± Standard deviation. n.s. p > 0.05; *p < 0.05; **p < 0.01. ACE-R, Addenbrooke’s Cognitive Examination-Revised; Digits-F, Digit Span Forwards (maximum span); Digits-B, Digit Span Backwards (maximum span); RCF, Rey Complex Figure. Missing scores: Digit Span: 2 PNFA; Sydney Language Battery Comprehension: 2 controls; Doors Test: 1 AD; RCF: 2 AD; Trail Making Test A: 2 PNFA; Trail Making Test B: 4 PNFA; Ekman 60:3 PNFA; 1 AD.

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diagnosis was present averaged across story versions and phases (F(2,32) = 15.704, p < 0.001) with the AD group demonstrating worse memory than the control (p < 0.001) and PNFA (p = 0.003) groups overall. A main effect of story version was also present (F(1,64) = 5.267, p = 0.028), with the emotional story remembered better than the neutral story averaged across groups. The interaction between Phase and Version was significant (F(2,64) = 4.091, p = 0.021), with Phase 2 of the emotional story remembered better than Phase 3 of the emotional story (p = 0.012) and Phase 2 of the emotional story also remembered better than Phase 2 of the neutral story (p = 0.001) averaged across groups. No other interactions between diagnosis, story version or phase were significant. Given the main effect of diagnosis and the a priori hypothesis of a differential effect of emotion on memory across groups, planned contrasts were conducted to investigate differences across diagnostic groups comparing emotional and neutral story performance for each phase. The PNFA group remembered a similar level of details from the emotional and neutral story (p > 0.05) averaged across phases (see Fig. 3). This was also the case when performance was examined in each phase separately (all p values >0.05). In contrast,

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(F(2,32) = 1.315, p > 0.05). Furthermore, the interaction between story version and diagnosis was not significant (F(2,32) = 0.294, p > 0.05), indicating that subjectively, both stories were understood to a similar degree across groups (Fig. 1). Examination of the subjective ratings of emotionality, shown in Fig. 2, revealed a significant main effect of story version (F(1,32) = 30.491, p < 0.001), with the emotional story rated as significantly more emotional than the neutral story. No main effect of diagnosis (F(2,32) = 2.388) or interaction between diagnosis and version (F(2,32) = 0.924, p > 0.05) was observed. Post hoc analyses indicated that PNFA (p = 0.015), AD (p = 0.006) and controls (p < 0.001) rated the emotional story significantly higher in emotionality than the neutral story. A marginally significant difference in the ratings of the neutral story was seen between PNFA and controls, with the PNFA group rating the neutral story as more emotional than controls (p = 0.048). No other between group differences were present.

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Fig. 2. Subjective ratings of emotionality in progressive nonfluent aphasia (PNFA) and Alzheimer’s disease (AD) patients compared to controls. Error bars represent standard error of the mean.

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Fig. 1. Subjective ratings of understanding in progressive nonfluent aphasia (PNFA) and Alzheimer’s disease (AD) patients compared to controls. Error bars represent standard error of the mean.

Memory performance The results for memory performance across the three groups according to story version and phase is shown in Fig. 3. A significant main effect of

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Fig. 3. Memory for the neutral and emotional story according to phase in progressive nonfluent aphasia (PNFA) and Alzheimer’s disease (AD) compared to controls. Error bars represent standard error of the mean.

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Relationship between emotional enhancement of memory, neuropsychological test performance, and caregiver burden

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groups. In PNFA, memory for the emotional story positively correlated with emotion recognition ability (r = 0.745, p = 0.007) and general cognition (r = 0.644, p = 0.009). In contrast, no associations between memory for the neutral story and neuropsychological test performance were present in this group. In AD, visual memory recall performance on the RCF was positively correlated with memory for the neutral story (r = 0.736, p = 0.005). No correlations between emotional story memory and neuropsychological performance, however, were observed in this patient group (Table 3). In addition, attention, naming and language comprehension, and a non-verbal executive functioning measure did not significantly correlate with performance on the emotional memory task in either group (Table 3). Examination of correlations between emotional memory task performance, disease severity and carer wellbeing revealed significant associations in the PNFA group only (Table 4). Worse memory for the emotional story correlated with increased carer depression (r = −0.682, p = 0.005) and stress (r = −0.697, p = 0.004) in the PNFA group. Performance on the neutral story was not significantly associated with carer wellbeing or burden in either group, with the exception of carer depression in PNFA, which was marginally significant (r = −0.646, p = 0.009). In addition, disease

Memory and emotion recognition ability were differentially associated with performance on the emotional enhancement of memory task across patient

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Table 3 Correlations between emotional enhancement of memory and neuropsychological test performance in progressive nonfluent aphasia (PNFA) and Alzheimer’s disease (AD) Cognition ACE-R Emotional Story Total % PNFA AD Neutral Story Total % PNFA AD

0.644* 0.512

Emotion

Attention

Doors A

Memory

RCF

Ekman 60

Digits Forward

Naming

Comp.

Trails B

0.485 0.663

0.150 0.496

0.745* 0.482

0.623 0.453

0.595 0.055

0.049 0.087

−0.182 −0.317

0.222 0.736*

0.695 0.638

0.543 0.575

0.616 0.210

0.227 −0.247

0.037 0.011

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controls remembered significantly more details from Phase 2 of the emotional story than the neutral story (p = 0.023), whereas memory for Phase 1 and Phase 3 of the two story versions were similar (p values >0.05). Further, performance in the control group on Phase 2 of the emotional story was significantly higher than Phase 3 (p = 0.032). No other differences in performance were present across phases according to story version in this group (all other p values >0.05). Similarly, the AD group remembered significantly more details in Phase 2 of the emotional story than the neutral story (p = 0.012), and this effect was also seen when performance was averaged across story phases (p = 0.036). Together, these results reveal that while controls and AD benefitted from emotional information, showing enhanced memory for the crucial phase of the emotional story, no effect of emotion on memory was present in PNFA.

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0.592 0.349

0.208 0.624

Language

Exec.

Values are Pearson correlation one-tailed. *p < 0.01. ACE-R, Addenbrooke’s Cognitive-Examination-Revised; Comp., Comprehension; Exec., Executive functioning. Missing data: Doors Test: 1 AD; RCF: 2 AD; Ekman 60:3 PNFA; 1 AD; Digit Span: 2 PNFA; Trail Making Test A: 2 PNFA; Trails Making Test B: 4 PNFA.

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Table 4 Correlations between emotional enhancement of memory and disease severity, carer wellbeing and carer burden in progressive nonfluent aphasia (PNFA) and Alzheimer’s disease (AD) Severity Emotional Story Total % PNFA AD Neutral Story Total % PNFA AD

Carer wellbeing (DASS)

Burden

FRS

Depression

Anxiety

Stress

Zarit

0.497 0.217

−0.682* 0.282

−0.550 0.268

−0.697* 0.271

−0.513 0.233

0.567 0.272

−0.646* −0.253

−0.400 −0.217

−0.627 −0.299

−0.597 −0.112

Values are Pearson correlation one-tailed t test. *p < 0.01. FRS, Functional rating Scale. FRS scores missing for 1 PNFA and 1 AD patient. Higher scores denote higher functioning. Carer mood assessed using the Depression, Anxiety and Stress Scale (DASS).

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This study is the first to examine emotional enhancement of memory using an engaging, ecologically valid task in PNFA in comparison to AD. The results reveal that emotional enhancement of memory is lost in PNFA, whereas in AD, emotion facilitates memory for naturalistic events. Correlation analyses show distinct associations between memory for emotional and neutral events and specific cognitive abilities that are exclusive to each patient group, and suggest that the differential effect of emotion on memory is due to distinct neurocognitive abnormalities present in these dementia syndromes. In PNFA, memory for the emotional story correlated with patients’ emotion recognition ability, suggesting that a primary emotion processing deficit underlies their impaired performance on both the emotion recognition and emotional memory tasks. Although previous studies have suggested that inattention and/or face perception deficits may contribute to reductions in emotion recognition in PNFA [24], we found no evidence of an association between attention and memory for the neutral or emotional story. It is possible that differences in task demands may determine the extent that inattention/face perception deficits influence performance. Here, we have demonstrated that for an engaging, naturalistic task, deficits in attention, or other cognitive abilities, do not correlate with emotional enhancement of memory in PNFA. Our results concur with the previous finding that simple visual recognition memory is not enhanced by emotion in PNFA [10]. Interactions between the amygdala and hippocampus (e.g., [2, 47, 48]) and to some extent the prefrontal cortex [49], are crucial for emotional enhancement of memory to proceed. Absence of emotional enhancement of memory in PNFA suggests that additional brain structures also play an important role in this phenomenon. The insula has widespread reciprocal connections with the amygdala [50] and is involved in autonomic function, perception and mood [51], and animal studies have demonstrated it is an important anatomical substrate for learning and memory [52]. It is therefore possible that damage to the insula, as is found in PNFA, prevents the

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DISCUSSION

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integration of information about autonomic arousal, emotion perception, and learning and memory, which impinges on emotional enhancement of memory. The inferior frontal gyrus also appears to be an important structure for emotional memory enhancement in these patients [10]. This region has previously been implicated in aspects of empathy [22] and is recruited with the amygdala and hippocampus during autobiographical memory retrieval [53]. The precise roles of the insula and inferior frontal gyrus in emotional enhancement of memory warrant closer investigation. Brain regions, necessary for emotional enhancement of memory are also affected in semantic dementia, the other language variant of frontotemporal dementia. Deficits in emotion recognition and empathy in these patients are well-documented [11, 54]. Like PNFA, the only study to date examining emotional memory in semantic dementia reported an absence of emotional enhancement in these patients [10]. Although ecological measures have not yet been applied in this subtype, it is likely that attenuation of emotional enhancement is also present in semantic dementia even under naturalistic conditions, reflecting the profound impact of neurodegeneration in the frontal and temporal lobes on emotion processing and social cognition. While neuroimaging analysis was beyond the scope of this study, our results provide important evidence of a primary emotion processing impairment that is associated with degradation of emotional enhancement of memory for complex ecologically valid events in PNFA. The pattern of results seen in AD is in contrast to those seen in PNFA, with AD patients demonstrating a facilitatory effect of emotion on memory, consistent with previous studies that have used naturalistic, engaging tasks to assess emotional memory in AD (e.g., [6]). Furthermore, evidence of an association between episodic memory ability and performance on the neutral story only provides insight into the mechanisms underpinning successful emotional memory enhancement in AD. While episodic memory capacity appears to determine the extent non-emotional information is remembered, it is not related to the capacity of emotion to enhance memory. This finding is in line with previous reports that emotional enhancement can proceed, even in cases where episodic memory ability is compromised, such as in amnesic patients [55]. Clinically, our results suggest that in day-to-day situations, AD patients have the capacity to harness emotional information to facilitate memory, especially in the early stages of the disease. The second aim of this study was to examine the extent performance on the emotional memory task

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severity was not significantly associated with memory for the neutral or emotional story in either group indicating that attenuation of emotional enhancement of memory between groups is not simply a function of disease severity.

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ACKNOWLEDGMENTS

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frontotemporal dementia subtypes [65, 66]. In summary, this is the first study to examine the effect of emotion on memory for a complex naturalistic event in PNFA in comparison with AD and has revealed that the enhancement effect is lost in PNFA patients. This absence of emotional enhancement adversely affects carer wellbeing, which warrants further investigation.

The authors are grateful to the participants and their families for supporting our research and Larry Cahill and James McGaugh for kindly providing the emotional memory task. This work was supported by funding to ForeFront, a collaborative research group dedicated to the study of frontotemporal dementia and motor neurone disease, from the National Health and Medical Research Council (NHMRC) of Australia program grant (1037746) and the Australian Research Council (ARC) Centre of Excellence in Cognition and its Disorders Memory Node (CE110001021); an ARC Federation Fellowship (FF0776229 to JRH); and an NHMRC Career Development Fellowship (APP1022684 to OP). Authors’ disclosures available online (http://www.jalz.com/disclosures/view.php?id=2228).

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was associated with carer wellbeing. The factors that impact on carer wellbeing have rarely been explored in PNFA [56]. Our results revealed for the first time that degradation of emotional enhancement of memory in PNFA is associated with increased levels of stress and depression in carers of these patients, whereas no associations were seen in AD. Carers of individuals with younger-onset dementia report reductions in psychological wellbeing and loneliness [57] as well as relationship difficulties and increased family conflict [58]. Although deficits in emotion recognition are associated with poor quality of social interactions and reduced ability to live independently [59, 60], the extent that emotional memory impairment impacts on functional abilities and carer wellbeing has been unexplored. Reductions in patients’ ability to remember evocative emotionally-relevant events, such as the death of a close friend or witnessing an accident, may contribute to loneliness and a loss of relationship satisfaction in the carer, and in turn increase carer stress and depression. Although the precise relationship between emotional enhancement of memory and carer wellbeing requires further investigation, this important finding has implications for the management of carer depression and stress. Despite the relatively small sample size of the current study, our results demonstrate distinct profiles of emotional memory across these dementia syndromes. Our results have also revealed robust correlations with cognitive profiles specific to each group. Whether emotional enhancement of memory for positive events is also compromised in PNFA remains to be determined. Some evidence suggests that memory for positive events may be more gist based and dependent on prefrontal rather than medial temporal regions [61–63]. Future studies should consider examining memory enhancement of both negative and positive events in PNFA, given the potential clinical relevance of emotional enhancement for positive events in these patients. In addition, deficits in emotion processing have only recently been identified in this patient group. Of relevance here, a recent study reported that performance on the “Reading the mind in the eyes” theory of mind test was impaired in PNFA, with patients performing at a similar level to individuals with the behavioral-variant of frontotemporal dementia [64]. Whether the observed impairments in emotion recognition, emotional enhancement of memory and theory of mind extend to other aspects of social cognition such a sarcasm detection is unclear although this possibility warrants investigation given existing evidence that these abilities are commonly affected in the other

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Ecological assessment of emotional enhancement of memory in progressive nonfluent aphasia and Alzheimer's disease.

Events which are imbued with emotion are typically remembered vividly and with more confidence than similar non-emotional events. The extent that emot...
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