Psychiatry Research 200 (2012) 361–367
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Anhedonia and emotional word memory in patients with depression Wen-hua Liu a,b, Ling-zhi Wang c, Su-hua Zhao c, Yu-ping Ning c, Raymond C.K. Chan d,n a
Faculty of Health Management, Guangzhou Medical College, Guangzhou, China Faculty of Life Sciences, Sun Yat-Sen University, Guangzhou, China Department of Clinical Psychology and Rehabilitation, Guangzhou Psychiatric Hospital, Guangzhou, China d Neuropsychology and Applied Cognitive Neuroscience Laboratory, Key Laboratory of Mental Health, Institute of Psychology, Chinese Academy of Sciences, Beijing, China b c
a r t i c l e i n f o
abstract
Article history: Received 30 January 2012 Received in revised form 23 June 2012 Accepted 16 July 2012
Anhedonia is a key diagnostic criterion for major depression. Investigating the relation between the specific symptoms and emotional processing may help to understand the underlying cognitive mechanism of anhedonia in depression. In this study, we explored the potential association between memory for emotional words and anhedonia in 71 patients with depression and 61 healthy individuals. An emotional word-rating task was administered to assess self-reported emotional experience to words on both valence and arousal dimensions, and subsequent recall and recognition memory for these words. Depressed patients demonstrated a reduction in pleasure and arousal experience to positive words, but an increase in arousal experience to negative words. Depressed patients also displayed a lower overall memory performance in recall measure and a bias to memory of more negative words. Moreover, state anhedonia and trait anhedonia were associated with attenuated positive experience and enhanced negative experience in patients with depression only. Higher levels of anhedonia and depression severity were also associated with fewer positive words and more negative words memory. Patients with depression displayed a flat pattern of emotional experience to positive stimuli and a tendency towards rating negative stimuli more intensely. & 2012 Elsevier Ireland Ltd. All rights reserved.
Keywords: Depression Anhedonia Memory Emotional processing
1. Introduction Anhedonia, defined as a reduced capacity to experience or pursue pleasure, is a main symptom of depression (APA, 1994). A rich literature has shed light on the ways that anhedonia could influence life function and increase vulnerability to the development of psychic disease (Chapman et al., 1994; Mason et al., 2004; Gooding et al., 2005); however, the underlying mechanisms by which these changes may occur are still not clearly known. One way to help understand this question is to determine the correlation between anhedonia and other cognitive processing of depression. Meehl suggested that hedonic capacity serves as a buffer against the negative influences of stress (Meehl, 1962). Anhedonia might change cognitive processing for emotional information in such a way that positive information is more difficult to retrieve and sustain than the negative information (Mathews and Barch, 2006). Hence, there will be less availability of cognitive or emotional resources to buffer against stressful or negative experiences. Indeed, findings have confirmed a range of cognitive deficits in patients with depression (Jaeger et al., 2006; n Correspondence to: Institute of Psychology, Chinese Academy of Sciences, 4A Datun Road, Beijing, China; Tel./fax: þ86(0)10 64836274. E-mail addresses:
[email protected],
[email protected] (R.C.K. Chan).
0165-1781/$ - see front matter & 2012 Elsevier Ireland Ltd. All rights reserved. http://dx.doi.org/10.1016/j.psychres.2012.07.025
Beblo et al., 2011; Elderkin-Thompson et al., 2011), and among these deficits, memory deficit is supposed to be a premorbid marker of depression (Airaksinen et al., 2007), and is found in particular sub-types of depressed patients (Burt et al., 1995). Preliminary findings also indicate that memory of positively valenced information can predict depressive symptomatic improvement (Johnson et al., 2007; Roy et al., 2010). Interestingly, despite the obvious abnormal affective features of the construct of anhedonia, little is known about memory for emotionally valenced information of individuals identified as high in anhedonia. Empirical findings show that decreased emotional experiences in the valence or arousal aspects have been demonstrated in healthy individuals with anhedonia (Mathews and Barch, 2006; Kerns et al., 2008; Leung et al., 2010), and such emotional experience abnormalities could influence the encoding processes relating to memory (Mickley Steinmetz and Kensinger, 2009; Mickley Steinmetz et al., 2010). Furthermore, it is also suggested that arousal and valence may work in distinct neural pathways to mediate the enhancing effect of emotion on memory formation (Kensinger, 2004; Kensinger and Corkin, 2004). In particular, arousal depends on an amygdalar–hippocampal network, whereas non-arousing valence is linked to a prefrontal cortex– hippocampal network (Kensinger and Corkin, 2004). To date, most studies have been limited to healthy samples. Although
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empirical findings indicate there is a reduction in the intensities of pleasure in depression (Watson and Naragon-Gainey, 2010), the relationship among anhedonia, emotional experience and memory in the individuals with major depression remains unclear. The current study sought to examine emotional response and memory performance in patients with depression compared to healthy individuals. We measured emotional experience and memory using an emotional word-rating method (Mathews and Barch, 2006), which required participants to rate emotional words on both valence and arousal dimensions, then immediately recall and recognize these words. We expected emotional experience in valence and arousal to be decreased and memory deficits to be increased in patients with depression compared with the healthy individuals. In addition, in a more tentative and exploratory way, we would like to examine, in the case of an association between memory deficit and anhedonia, which types of anhedonia (e.g., state or trait anhedonia) might be responsible for this association.
The Snaith–Hamilton Pleasure Scale (SHAPS) (Snaith et al., 1995) was used to assess the state of anhedonia of the participants. The SHAPS is a 14-item checklist to assess an individual’s pleasure experience in the recent days. The Chinese translation of the SHAPS (SHAPS-C) showed excellent internal consistency in this sample, with an alpha of 0.95. The Temporal Experience of Pleasure Scale (TEPS) (Gard et al., 2006) was used to evaluate the long-term experience of pleasure among the participants. The TEPS includes two subscales, anticipatory pleasure scale (TEPS-ANTI) which measures the pleasure experienced in anticipation of a positive stimulus and consummatory pleasure scale (TEPS-CON) which measures the online, in-the-moment pleasure in response to a stimulus. The study used a 20-item Chinese version, which has been proved to possess adequate reliability (Chan et al., 2010; Chan et al., 2012a; Chan et al., 2012b). The Cronbach’s alphas for TEPS-ANTI and TEPS-CON in the current sample were 0.70 and 0.78, respectively. The BDI (Beck et al., 1961) was widely used to assess the severity of depressive symptoms in the past 2 weeks. The Chinese version of BDI has excellent psychometric properties (Wang et al., 1999) and the Cronbach’s alpha in the current sample for BDI was 0.95.
2. Materials and method
The study was approved by the ethics committees of the Guangzhou Psychiatric Hospital and written informed consent was obtained from all of the participants. After completing the self-reported measures, the emotional wordrating task was administered to each participant in a quiet room in hospital.
2.3. Emotion assessment instruments
2.4. Procedure
2.1. Participants Seventy-one outpatients with depression (52.1% males; age: 27.33 7 8.90 years) were recruited to this study from a local psychiatric hospital, the Guangzhou Psychiatric Hospital, in China. Based on hospital records, patients with depression were enrolled if they met the diagnosis for major depressive disorder according to the Diagnostic and Statistical Manual, Fourth Edition (DSMIV) (APA, 1994). Patients with any other concurrent Axis I disorders, current or past psychotic features, neurological disorders, substance abuse and electroconvulsive therapy in the previous 6 months were excluded. Addition entry criteria into the study for patients required a score of 416 on the Beck Depression Rating Scale (Beck et al., 1961). The mean Beck Depression Inventory (BDI) score for the patients was 27.87 (standard deviation (S.D.)¼ 7.60; range 17–49). The average length of illness was 2.34 years (S.D. ¼ 3.07) and the cumulative duration treated was 9.18 months (S.D. ¼ 10.09) for the patients. Sixty-one healthy individuals (50.80% males; age: 26.11 7 5.65 years) were recruited from the local community and were screened by the experienced psychiatrists to ascertain the healthy controls did not have psychiatric or neurologic disorders. The mean BDI score for the healthy controls was 2.72 (S.D. ¼2.28; range 0–9).
2.2. Emotional word-rating task The words for this task were selected from those used in previous research (Mathews and Barch, 2006) and from those rated high frequency of occurrence in Frequency Dictionary of Chinese Words. An initial set of words (50 positively, 50 negatively and 50 neutrally valenced words) were selected according to equated word frequency and same word length. Then, the affective valence and arousal of these words were rated by 20 undergraduates, using a 9-point scale to report the levels of emotional pleasantness and arousal. Based on acquired valence and arousal ratings, five categories of 20 words (neutral, positive-high arousal, positive-low arousal, negative-high arousal and negative-low arousal words) were chosen. Analysis of variance (ANOVA) showed there were significant differences between the five categories of words in the valence (F(4,95)¼ 396.824, P o 0.001) and arousal variable (F(4,95)¼16.60, Po 0.001), and categories did not differ significantly in word frequency (F(4,95)¼ 1.40, P ¼ 0.24). These words were randomly selected into two sets of words, each of which comprised five categories of 10 words. One of the sets (target words) was presented in the whole task and one of the sets (distracter words) was included in the recognition measure. The words were presented in different random orders for every participant. Participants used a 9-point scale to report how pleasant (range: 1¼ extremely unpleasant; 9¼ extremely pleasant) and arousing (range: 1 ¼not at all arousing; 9¼ extremely arousing) each word was. After finishing the word ratings, each participant was asked to recall and write the words on a sheet of paper in 5 min, as many as possible. Finally, participants were given a list of 100 words of which 50 were the target words and 50 were distracters. For each word, participants were asked to indicate which words they had previously rated. The dependent variable for recall and recognition measure was the number of words recalled and recognition d0 (Mathews and Barch, 2006). The recognition d0 (d0 ¼ Z(hits) Z(false alarm)) is a measure of discriminability between the old and new stimuli, which was described elsewhere (Ramponi et al., 2010).
2.5. Data analysis A 2 (group: depressed group, healthy controls) 5 (word type: neutral, positivehigh arousal, positive-low arousal, negative-high arousal and negative-low arousal words) ANOVA was used to examine whether the patients with depression differed from the healthy controls in the word ratings and memory performance, with group as a between-subject factor, and word type as within-subject factor. The Greenhouse–Geisser correction was used for the ANOVAs where applicable, and post hoc Bonferroni tests were performed in cases of significant ANOVA effects. Pearson correlation analysis was run between the SHAPS, TEPS, BDI and the level of recall and recognition d0 to examine the association of anhedonia, depression severity and memory performance in the patients with depression. To test a possible specific link between anhedonia and memory performance, hierarchical regression analysis was run to evaluate if anhedonia (measured by the SHAPS and TEPS) uniquely predicted memory performance during recall and recognition measures after controlling BDI measure of depression severity (entered in the first step).
3. Results 3.1. Demographic and emotional information There were no significant differences between groups on demographic variables. The patients with depression demonstrated significantly higher levels of depressive symptoms, state and trait anhedonia than the healthy controls (Table 1). 3.2. Valence and arousal ratings ANOVA for the valence ratings revealed a main effect of word type (F(4,520) ¼1300.843, Po0.001, partial Z2 ¼0.909) and interaction of word type group (F(4,520) ¼3.627, P¼0.031, partial Z2 ¼0.027). Post hoc analysis for interaction indicated that the two groups rated negative words as more negative and positive words as more positive than neutral words (all P’s o0.001), and compared to the control group, the depressed group rated neutral, positive-low arousal and positive-high arousal words as more negative(all P’so0.05) (Fig. 1). ANOVA for the arousal ratings revealed a main effect of word type (F(4,520)¼ 76.763, Po0.001, partial Z2 ¼0.371) and interaction of word type group (F(4,520) ¼8.613, Po0.001, partial Z2 ¼0.062). Post hoc analysis for interaction indicated that the two groups rated neutral words as less arousing than negative-high arousal, positive-high arousal and positive-low arousal words
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Table 1 Demographic and emotional variables for patients with depression and healthy controls. Patients with depression (N¼ 71)
Healthy controls (N ¼61)
Statistics
Demographic characteristics Gender (M/F) Age (years) Education (years) Estimated I.Q. (WASI) BDI(0–63) SHAPS(14–56) TEPS total score TEPS-ANTI(11–66) TEPS-CON(9–54)
37/34 27.33 7 8.90 13.05 72.85 107.15 7 13.89 27.87 7 7.60 28.80 76.94 66.09 715.35 37.30 79.58 29.19 7 7.28
31/30 26.11 7 5.65 13.49 7 1.68 108.52 7 8.99 2.72 72.28 20.83 75.36 86.33 7 11.43 46.89 7 6.43 39.44 7 6.92
X¼ 0.01,p 40.05 t(130) ¼ 0.92,p ¼0.35 t(130) ¼ 1.04,p¼ 0.30 T(130) ¼ 0.66,p ¼0.51 t(130) ¼ 24.88,p o 0.001 t(130) ¼ 7.28,p o 0.001 t(130) ¼ 8.21,p o0.001 t(130) ¼ 6.55,p o0.001 t(130) ¼ 8.16,p o0.001
Clinical characteristics Duration of illness (years) Cumulative duration treated(months)
2.34 73.07 9.18 710.09
Data are presented as n or mean 7 SD. Notes: BDI: Beck Depression Inventory; SHAPS: Snaith-Hamilton Pleasure Scale; TEPS-ANTI: Temporal Experience of Pleasure Scale – Anticipatory Pleasure Subscale; TEPS-CON: Temporal Experience of Pleasure Scale – Consummatory Pleasure Subscale.
3.3. Recall and recognition For the recall measure, ANOVA revealed a main effect of word type (F(4,520)¼60.035, Po0.001, partial Z2 ¼0.316) and interaction of word type group (F(4,520)¼ 10.380, Po0.001, partial Z2 ¼0.074). Post hoc analysis for interaction indicated that the two groups recalled more high-arousal than low-arousal words (all P0 so0.05), and the control group recalled more positive-high arousal words (3.36170.17) than negative-low arousal words (1.44370.15) (P o0.001), while the depressed group did not. In addition, compared to the control group, the depressed group recalled significantly fewer neutral, negative-high arousal, positive-low arousal and positive-high arousal words (all P0 so0.001) (Fig. 3). For the recognition d0 , no significant result emerged (all P0 s40.60).
9 8
* *
6
*
5 4 3 2 1 0
Negative High Arousal
Negative Low Arousal
Neutral
Positive Low Arousal
Positive High Arousal
Fig. 1. The valence ratings in the depressed group and control group for five types of words. Error bars represent the standard error. Asterisks indicate significant difference between the groups (Po 0.05).
3.4. Relationship between clinical characteristics, emotional experience and memory performance
9 8 7 Degree of arousal
For the patients with depression, high levels of state anhedonia (measured by SHAPS) were associated with attenuated pleasant experience of positive-high and positive-low arousal words, and attenuated arousal experience of positive-high arousal words (all P0 s o0.05), high levels of trait anhedonia (measured by TEPS and TEPS-ANTI) were associated with enhanced arousal experience of negative-high and negative-low arousal words(all P0 so0.05), TEPS–CON measure of consummatory anhedonia and BDI measure of depressive symptoms were associated with enhanced arousal experience of negative-high arousal words (all P0 so0.01) (Table 2). Further, regression analysis showed that TEPS–ANTI measure of anticipatory anhedonia uniquely predicted the arousal rating of negative-high arousal words (DR2 ¼0.34, DF(2,68)¼17.840, Po0.001) after controlling for BDI measure of depression severity. For the recall measure, high levels of trait anhedonia (measured by TEPS, TEPS–ANTI and TEPS–CON) in the patients with depression were associated with poor recall for positive-low
Depressed group Control group
7
Degree of valence
(all P’so0.001), but not significantly different from negative-low arousal words (all P0 s40.06). Further, compared to the control group (negative-high arousal words: 5.54670.19; positive-high arousal words:7.10370.13), the depressed group rated negativehigh arousal words (6.38070.18) as more arousing and rated positive-high arousal words (6.28970.12) as less arousing (all P0 so0.001) (Fig. 2).
Depressed group Control group * *
6 5 4 3 2 1 0 Negative High Arousal
Negative Low Arousal
Neutral
Positive Low Arousal
Positive High Arousal
Fig. 2. The arousal ratings in the depressed group and control group for five types of words. Error bars represent the standard error. Asterisks indicate significant difference between the groups (Po 0.05).
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5 4.5
*
Number Recalled
4
Depressed group Control group
3.5 3
*
*
2.5 2
*
1.5 1 0.5 0
Negative High Arousal
Negative Low Arousal
Neutral
Positive Low Arousal
Positive High Arousal
Fig. 3. Number of words recalled for depressed group and control group. Error bars represent the standard error. Asterisks indicate significant difference between the groups (Po 0.05).
arousal words (all P0 so0.05), and high levels of trait anhedonia (measured by TEPS–CON) in the depressed patients were associated with poor recall for neutral words (P¼0.03). Moreover, the patients with higher depression severity also showed a trend for recalling more negative low-arousal words (r ¼0.21, P¼0.06). For the recognition measure, both high levels of state anhedonia (measured by SHAPS) and trait anhedonia (measured by TEPS, TEPS–ANTI and TEPS–CON) in the patients were associated with poor recognition of positive-high arousal words (all P0 s o0.05) (Table 3). Highlighting the specificity of these findings, regression analysis clarified that TEPS measure of anhedonia predicted recall of positive low-arousal words (DR2 ¼0.10, DF(2,68)¼3.792, p ¼0.027), TEPS–CON measure of consummatory anhedonia predicted recall of neutral words (DR2 ¼0.08, DF(2,68)¼3.193, P¼0.047), and TEPS–ANTI measure of anticipatory anhedonia predicted recognition of positive high-arousal words (DR2 ¼0.16, DF(2,68)¼ 6.742, P¼0.002) after controlling for BDI measure of depression severity.
4. Discussion The study used an emotional word-rating task to explore the difference between the patients with depression and the healthy individuals in the emotional experience and memory performance, with particular focus on the role of anhedonia in emotional processing. The current findings showed that (1) the patients with depression demonstrated attenuated emotional experience to positive words both in pleasant and arousal aspects, and enhanced arousal experience to negative words compared with the healthy controls, (2) the patients with depression showed overall poorer recall memory compared with the healthy controls and anhedonia in the patients were associated with poor memory of positive words and (3) for the role of anhedonia in emotional processing, state anhedonia and trait anhedonia were linked to attenuated experience to positive words and enhanced experience to negative words, respectively, and trait anhedonia uniquely predicted the memory of positive words and the arousal experience of negative words.
Consistent with our hypothesis and previous findings, patients with depression displayed reduced emotional valence and arousal experience in response to positive emotional stimuli relative to the healthy individuals (Fitzgibbons and Simons, 1992; Fiorito and Simons, 1994). Our current findings also showed that emotional response in depression was characterised by an enhanced arousal experience of highly arousing negative stimuli, although these was no group differences in pleasant experience of negative stimuli. Up to now, few studies examined self-reports of emotional experience in arousal aspect. Some studies examine the physical arousal response to emotional stimuli, but results are mixed. For example, one study found that patients with depression and healthy individuals possessed similar changes in autonomic physical arousal response (e.g., skin conductance response) when exposed to emotional stimuli (Rottenberg et al., 2005). However, another study argued that the severely depressed patients, but not mildly depressed patients, possessed deficit in affective startle response (Kaviani et al., 2004). The reason for these discrepancies might be due to varied depression severity across samples. Moreover, depressed patients often vary widely in their extent of co-morbid anxiety, a factor known to influence physical response, which may lead to increased arousal response to a negative stimulus. In addition, consistent with previous studies investigating recall and recognition memory in depression (Neshat-Doost et al., 1998; Jermann et al., 2009), the patients with depression demonstrated poorer recall memory but not recognition memory than the healthy individuals. The possibility is that the memory deficit of depression is restricted to impaired conscious retrieval from memory or high effort-demanding implicit memory measure (Brand et al., 1992). As a more automatically performed task, the recognition measure in this study might be less sensitive than the recall measure to the patients with depression. Further, this study showed that anhedonia in the patients with depression was associated with poor memory for positive words, which is consistent with recent studies indicating that depressed individuals are less responsive to a range of positive stimuli than nondepressed controls (Henriques et al., 1994; Sloan et al., 2001; Suslow et al., 2001; Joormann and Gotlib, 2006; Pizzagalli et al., 2009; Gotlib et al., 2011). Because research has suggested that arousal has a bigger influence than valence on whether a stimulus is remembered (Bradley et al., 1992), the attenuated memory to positive words is possibly due to the decreased arousal experience to positive stimuli for those severely depressed patients. This study is one of the few studies to examine the role of state anhedonia and two types of trait anhedonia on emotional processing in the patients’ sample. Since anhedonia has been suggested as a dichotomous entity (Blanchard et al., 2000), some differences may be diminished in prior healthy sample (Mathews and Barch, 2006), especially when the range of this deficit might be narrow or the relationship with cognitive processing is possibly nonlinear. When the independent contribution of each type of anhedonia to emotional experience was examined, results revealed that state anhedonia was associated with reduced pleasant and arousal experience of positive emotional words, while trait anhedonia was linked to increased arousal experience of negative emotional words. Further, after controlling the effect of depression severity, TEPS measure of trait anhedonia, but not SHAPS measure of state anhedonia, uniquely predicted the memory of positive words and the arousal experience of negative words. It seems that the disturbances in memory for affective stimuli are due to the lasting abnormal emotional experience. However, the presence of memory impairments may influence patients’ reports of pleasurable experience in a reversed way, causing them to access semantic memory and base their identityrelated information instead of the current stimuli of emotion
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Table 2 Relationship between anhedonia and word valence and arousal ratings in patients with depression (n¼ 71). Criteria
Valence rating
Arousal rating
Negative high arousal
Negative low arousal
Positive high arousal
Positive low arousal
Neutral Negative high arousal
Negative low arousal
Positive high arousal
Positive low arousal
Neutral
BDI
0.01 P¼ 0.99
0.03 P ¼0.92
0.11 P ¼ 0.36
0.06 P¼ 0.58
0.01 0.30nn P ¼0.92 P o 0.01
0.09 P ¼0.41
0.12 P ¼0.33
0.05 P¼ 0.66
0.10 P ¼0.39
SHAPS
0.09 P¼ 0.47
0.09 P ¼0.45
0.34nn P o 0.01
0.24n P¼ 0.04
0.15 0.12 P ¼0.21 P ¼ 0.29
0.08 P ¼0.50
0.24n P ¼0.04
0.19 P¼ 0.10
0.01 P ¼0.93
TEPS
0.02 P¼ 0.84
0.12 P ¼0.29
0.16 P ¼ 0.17
0.18 P¼ 0.12
0.14 0.50nnn P ¼0.24 P o 0.001
0.24n P ¼0.04
0.13 P ¼0.27
0.08 P¼ 0.49
0.02 P ¼0.84
TEPS ANTI 0.03 P¼ 0.81
0.12 P ¼0.32
0.13 P ¼ 0.26
0.16 P¼ 0.16
0.12 0.56nnn P ¼0.30 P o 0.001
0.26n P ¼0.03
0.18 P ¼0.13
0.14 P¼ 0.22
0.08 P ¼0.49
TEPS CON
0.11 P ¼0.36
0.17 P ¼ 0.15
0.17 P¼ 0.14
0.13 0.32nn P ¼0.28 P o 0.01
0.18 P ¼0.14
0.04 P ¼0.75
0.02 P¼ 0.88
0.06 P ¼0.62
0.09 P¼ 0.47
Notes: BDI: Beck Depression Inventory; SHAPS: Snaith-Hamilton Pleasure Scale; TEPS-ANTI: Temporal Experience of Pleasure Scale – Anticipatory Pleasure Subscale; TEPS-CON: Temporal Experience of Pleasure Scale – Consummatory Pleasure Subscale. n
Indicates p o 0.05. Indicates P o0.01. Indicates P o0.001.
nn
nnn
Table 3 Relationship between anhedonia and memory performance in patients with depression (n ¼71). Criteria
Recognition (d0 )
Recall Negative high arousal
Negative low arousal
Positive high arousal
Positive low arousal
Neutral Negative high arousal
Negative low arousal
Positive high arousal
Positive low arousal
Neutral
BDI
0.06 P¼ 0.63
0.21 P ¼0.06
0.01 P ¼ 0.91
0.03 P¼ 0.78
0.17 0.02 P ¼0.14 P ¼ 0.84
0.09 P ¼0.44
0.14 P ¼0.25
0.04 P¼ 0.76
0.06 P ¼0.59
SHAPS
0.05 P¼ 0.65
0.05 P ¼0.67
0.17 P ¼ 0.15
0.16 P¼ 0.16
0.12 0.02 P ¼0.30 P ¼ 0.84
0.17 P ¼0.14
0.25n P ¼0.04
0.14 P¼ 0.23
0.03 P ¼0.77
TEPS
0.04 P¼ 0.70
0.04 P ¼0.69
0.20 P ¼ 0.09
0.32nn Po 0.01
0.22 0.08 P ¼0.06 P ¼ 0.48
0.18 P ¼0.13
0.40nnn P o 0.001
0.05 P¼ 0.69
0.13 P ¼0.27
TEPS ANTI 0.06 P¼ 0.57
0.03 P ¼0.79
0.18 P ¼ 0.13
0.28n P¼ 0.02
0.16 0.12 P ¼0.16 P ¼ 0.29
0.13 P ¼0.27
0.40nnn P o 0.001
0.08 P¼ 0.46
0.12 P ¼0.30
TEPS CON
0.06 P ¼0.62
0.18 P ¼ 0.12
0.29nn P¼ 0.02
0.26n 0.01 P ¼0.03 P ¼ 0.91
0.20 P ¼0.09
0.31nn P o 0.01
0.01 P¼ 0.88
0.11 P ¼0.33
0.18 P¼ 0.12
Notes: BDI: Beck Depression Inventory; SHAPS: Snaith-Hamilton Pleasure Scale; TEPS-ANTI: Temporal Experience of Pleasure Scale – Anticipatory Pleasure Subscale; TEPS-CON: Temporal Experience of Pleasure Scale – Consummatory Pleasure Subscale. Indicates p o 0.05. Indicates P o0.01. nnn Indicates P o0.001. n
nn
knowledge. Further studies are needed to help shed light on the relationship between anhedonia and memory impairment in patients with depression. The detached influences of different types of anhedonia on the emotional processing in patients with depression are worth noting when considering literatures suggested that anhedonia should no longer be considered only a diminished ‘capacity’ for pleasure, which may include some components linked to reward related or cognitive processes, for example, reward valuation, anticipation and motivation, decision making (Treadway and Zald, 2011; Der-Avakian and Markou, 2012), reduced pleasureseeking behaviour and beliefs of low pleasure (Strauss, 2012). For the neural bases of the construct of anhedonia, the ventral striatum and orbitofrontal cortex are thought to serve experiences of pleasure (Keedwell et al., 2005), and multiple reciprocal connections between different PFC subregions, as well as reciprocal connections of the ventral tegmental area, the nucleus accumbens, amygdala and hippocampus further contribute to other reward-related processes (Der-Avakian and Markou, 2012). Additional neurotransmitter,for example, glutamate/glutamine and
gamma-aminobutyric acid levels in prefrontal regions including the anterior cingulate cortex, also play an important role in regulating the behavioural response to rewards (Hasler et al., 2007; Walter et al., 2009; Gabbay et al., 2012). Although it is still not clearly known about the underlying neural mechanism linking anhedonia and memory deficits in patients with depression, a study in schizophrenia has suggested that cognitive impairments of encoding and retrieval processes that serve to maintain the beliefs of low pleasure may influence reports of non-current pleasurable experiences (Strauss, 2012). Future study should adopt neuroimaging or event-related potential paradigm to examine the corresponding neural network corresponding to the current findings. The current study has a number of limitations. First, some patients were taking different medications at the time of testing. The effects of medication on memory performance for emotional material still remain to be clarified. A second limitation concerns that some important effects may have gone undetected due to the correlational design. Entry criteria into the study rule out some mild depression, which may have further limited the size of the
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correlations. Clearly, these results require replication before firmer conclusions can be drawn. Finally, this study used an incidental encoding task and participants recall words with no delay after finishing word rating. There is evidence that the effect of emotion on memory can differ with time (Sharot and Yonelinas, 2008), and severely depressed patients displayed better delayed recall of positive than negative affect words, although their overall memory performance was poor (Calev, 1996). If this is the case, future studies will be needed to evaluate the different time courses for memory of emotional stimulus in depressed samples. Despite these limitations, the results of this study are suggestive of an abnormal pattern of emotional processing in patients with depression. The emotional experience associated with depression might have resulted in a differential deficit in positive and negative word memory.
Role of funding sources The funding agents had no further role in the study design; in the collection, analysis and interpretation of the data; in the writing of the manuscript; and in the decision to submit the paper for publication.
Contributors WHL designed the study, analysed the data and wrote up the first draft of the manuscript. LZW, SHZ and YPN administered tests and clinical ratings to patients and healthy controls. RCKC designed the study and wrote up the first draft of the manuscript. All contributors read the final version of the manuscript and agreed for submission.
Acknowledgements This study was supported partially by National Science Fund China Young Investigator Award (81088001), the Knowledge Innovation Project of the Chinese Academy of Sciences (KSCX2EW-J-8) and the Guangdong Natural Science Foundation (112004) and Guangzhou Education Bureau (10A253). References Airaksinen, E., Wahlin, A., Forsell, Y., Larsson, M., 2007. Low episodic memory performance as a premorbid marker of depression: evidence from a 3-year follow-up. Acta Psychiatrica Scandinavica 115, 458–465. APA, 1994. Diagnostic and Statistical Manual of Mental Disorders: DSM-IV, 4 ed. American Psychiatric Association, Washington DC. Beblo, T., Sinnamon, G., Baune, B.T., 2011. Specifying the neuropsychology of affective disorders: clinical, demographic and neurobiological factors. Neuropsychology Review 21, 337–359. Beck, A.T., Ward, C.H., Mendelson, M., Mock, J., Erbaugh, J., 1961. An inventory for measuring depression. Archives of General Psychiatry 4, 561–571. Blanchard, J.J., Gangestad, S.W., Brown, S.A., Horan, W.P., 2000. Hedonic capacity and schizotypy revisited: a taxometric analysis of social anhedonia. Journal of Abnormal Psychology 109, 87–95. Bradley, M.M., Greenwald, M.K., Petry, M.C., Lang, P.J., 1992. Remembering pictures: pleasure and arousal in memory. Journal of Experimental Psychology. Learning, Memory, and Cognition 18, 379–390. Brand, A.N., Jolles, J., Gispen-de Wied, C., 1992. Recall and recognition memory deficits in depression. Journal of Affective Disorders 25, 77–86. Burt, D.B., Zembar, M.J., Niederehe, G., 1995. Depression and memory impairment: a meta-analysis of the association, its pattern, and specificity. Psychological Bulletin 117, 285–305. Calev, A., 1996. Affect and memory in depression: evidence of better delayed recall of positive than negative affect words. Psychopathology 29, 71–76. Chan, R.C., Wang, Y., Huang, J., Shi, Y., Hong, X., Ma, Z., Li, Z., Lai, M.K., Kring, A.M., 2010. Anticipatory and consummatory components of the experience of
pleasure in schizophrenia: Cross-cultural validation and extension. Psychiatry Research 175, 181–183. Chan, R.C.K., Shi, Y.F., Lai, M.K., Wang, Y.N., Wang, Y., Kring, A.M., 2012a. The Temporal Experience of Pleasure Scale (TEPS): Exploration and confirmation of factor structure in a healthy Chinese sample. PLoS ONE 7 (4), e35352, http:// dx.doi.org/10.1371/journal.pone.0035352. Chan, R.C.K., Wang, Y., Yan, C., Zhao, Q., McGrath, J., His, X.L., Stone, W.S., 2012b. A study of trait anhedonia in non-clinical Chinese samples: Evidence from the Chapman Scales for Physical and Social Anhedonia. PLoS ONE 7 (4), e34275 http://dx.doi.org/10.1371/journal.pone.0034275. Chapman, L.J., Chapman, J.P., Kwapil, T.R., Eckblad, M., Zinser, M.C., 1994. Putatively psychosis-prone subjects 10 years later. Journal of Abnormal Psychology 103, 171–183. Der-Avakian, A., Markou, A., 2012. The neurobiology of anhedonia and other reward-related deficits. Trends in Neurosciences 35, 68–77. Elderkin-Thompson, V., Moody, T., Knowlton, B., Hellemann, G., Kumar, A., 2011. Explicit and implicit memory in late-life depression. American Journal of Geriatric Psychiatry 19, 249–255. Fiorito, E.R., Simons, R.F., 1994. Emotional imagery and physical anhedonia. Psychophysiology 31, 513–521. Fitzgibbons, L., Simons, R.F., 1992. Affective response to color-slide stimuli in subjects with physical anhedonia: a three-systems analysis. Psychophysiology 29, 613–620. Gabbay, V., Mao, X., Klein, R.G., Ely, B.A., Babb, J.S., Panzer, A.M., Alonso, C.M., Shungu, D.C., 2012. Anterior cingulate cortex gamma-aminobutyric acid in depressed adolescents: relationship to anhedonia. Archives of General Psychiatry 69, 139–149. Gard, D.E., Gard, M.G., Kring, A.M., John, O.P., 2006. Anticipatory and consummatory components of the experience of pleasure: A scale development study. Journal of research in personality 40, 1086–1102. Gooding, D.C., Tallent, K.A., Matts, C.W., 2005. Clinical status of at-risk individuals 5 years later: further validation of the psychometric high-risk strategy. Journal of Abnormal Psychology 114, 170–175. Gotlib, I.H., Jonides, J., Buschkuehl, M., Joormann, J., 2011. Memory for affectively valenced and neutral stimuli in depression: Evidence from a novel matching task. Cognition and Emotion, 1–9. Hasler, G., van der Veen, J.W., Tumonis, T., Meyers, N., Shen, J., Drevets, W.C., 2007. Reduced prefrontal glutamate/glutamine and gamma-aminobutyric acid levels in major depression determined using proton magnetic resonance spectroscopy. Archives of General Psychiatry 64, 193–200. Henriques, J.B., Glowacki, J.M., Davidson, R.J., 1994. Reward fails to alter response bias in depression. Journal of Abnormal Psychology 103, 460–466. Jaeger, J., Berns, S., Uzelac, S., Davis-Conway, S., 2006. Neurocognitive deficits and disability in major depressive disorder. Psychiatry Research 145, 39–48. Jermann, F., Van der Linden, M., Laurenc- on, M., Schmitt, B., 2009. Recollective Experience During Recognition of Emotional Words in Clinical Depression. Journal of Psychopathology and Behavioral Assessment 31, 27–35. Johnson, S.L., Joormann, J., Gotlib, I.H., 2007. Does processing of emotional stimuli predict symptomatic improvement and diagnostic recovery from major depression? Emotion 7, 201–206. Joormann, J., Gotlib, I.H., 2006. Is this happiness I see? Biases in the identification of emotional facial expressions in depression and social phobia. Journal of Abnormal Psychology 115, 705–714. Kaviani, H., Gray, J.A., Checkley, S.A., Raven, P.W., Wilson, G.D., Kumari, V., 2004. Affective modulation of the startle response in depression: influence of the severity of depression, anhedonia, and anxiety. Journal of Affective Disorders 83, 21–31. Keedwell, P.A., Andrew, C., Williams, S.C., Brammer, M.J., Phillips, M.L., 2005. The neural correlates of anhedonia in major depressive disorder. Biological Psychiatry 58, 843–853. Kensinger, E.A., 2004. Remembering emotional experiences: the contribution of valence and arousal. Reviews in the Neurosciences 15, 241–251. Kensinger, E.A., Corkin, S., 2004. Two routes to emotional memory: distinct neural processes for valence and arousal. Proceedings of the National Academy of Sciences of the United States of America 101, 3310–3315. Kerns, J.G., Docherty, A.R., Martin, E.A., 2008. Social and physical anhedonia and valence and arousal aspects of emotional experience. Journal of Abnormal Psychology 117, 735–746. Leung, W.W., Couture, S.M., Blanchard, J.J., Lin, S., Llerena, K., 2010. Is social anhedonia related to emotional responsivity and expressivity? A laboratory study in women. Schizophrenia Research 124, 66–73. Mason, O., Startup, M., Halpin, S., Schall, U., Conrad, A., Carr, V., 2004. Risk factors for transition to first episode psychosis among individuals with ‘at-risk mental states’. Schizophrenia Research 71, 227–237. Mathews, J.R., Barch, D.M., 2006. Episodic memory for emotional and nonemotional words in individuals with anhedonia. Psychiatry Research 143, 121–133. Meehl, P.E., 1962. Schizotaxia, schizotypy, schizophrenia. American Psychologist 17, 827–838. Mickley Steinmetz, K.R., Addis, D.R., Kensinger, E.A., 2010. The effect of arousal on the emotional memory network depends on valence. Neuroimage 53, 318–324. Mickley Steinmetz, K.R., Kensinger, E.A., 2009. The effects of valence and arousal on the neural activity leading to subsequent memory. Psychophysiology 46, 1190–1199.
W.-h. Liu et al. / Psychiatry Research 200 (2012) 361–367
Neshat-Doost, H.T., Taghavi, M.R., Moradi, A.R., Yule, W., Dalgleish, T., 1998. Memory for emotional trait adjectives in clinically depressed youth. Journal of Abnormal Psychology 107, 642–650. Pizzagalli, D.A., Iosifescu, D., Hallett, L.A., Ratner, K.G., Fava, M., 2009. Reduced hedonic capacity in major depressive disorder: evidence from a probabilistic reward task. Journal of Psychiatric Research 43, 76–87. Ramponi, C., Murphy, F.C., Calder, A.J., Barnard, P.J., 2010. Recognition memory for pictorial material in subclinical depression. Acta Psychologica 135, 293–301. Rottenberg, J., Gross, J.J., Gotlib, I.H., 2005. Emotion Context Insensitivity in Major Depressive Disorder. Journal of Abnormal Psychology 114, 627–639. Roy, M., Harvey, P.O., Berlim, M.T., Mamdani, F., Beaulieu, M.M., Turecki, G., Lepage, M., 2010. Medial prefrontal cortex activity during memory encoding of pictures and its relation to symptomatic improvement after citalopram treatment in patients with major depression. Journal of Psychiatry and Neuroscience 35, 152–162. Sharot, T., Yonelinas, A.P., 2008. Differential time-dependent effects of emotion on recollective experience and memory for contextual information. Cognition 106, 538–547. Sloan, D.M., Strauss, M.E., Wisner, K.L., 2001. Diminished response to pleasant stimuli by depressed women. Journal of Abnormal Psychology 110, 488–493.
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Snaith, R.P., Hamilton, M., Morley, S., Humayan, A., Hargreaves, D., Trigwell, P., 1995. A scale for the assessment of hedonic tone the Snaith-Hamilton Pleasure Scale. The British Journal of Psychiatry 167, 99–103. Suslow, T., Junghanns, K., Arolt, V., 2001. Detection of facial expressions of emotions in depression. Perceptual and Motor Skills 92, 857–868. Treadway, M.T., Zald, D.H., 2011. Reconsidering anhedonia in depression: lessons from translational neuroscience. Neuroscience and Biobehavioral Reviews 35, 537–555. Walter, M., Henning, A., Grimm, S., Schulte, R.F., Beck, J., Dydak, U., Schnepf, B., Boeker, H., Boesiger, P., Northoff, G., 2009. The relationship between aberrant neuronal activation in the pregenual anterior cingulate, altered glutamatergic metabolism, and anhedonia in major depression. Archives of General Psychiatry 66, 478–486. Wang, X.D., Wang, X.L., Ma, H., 1999. Rating Scales for Mental Health Chinese Mental Health Journal 12, 431–434. Watson, D., Naragon-Gainey, K., 2010. On the specificity of positive emotional dysfunction in psychopathology: evidence from the mood and anxiety disorders and schizophrenia/schizotypy. Clinical Psychology Review 30, 839–848.