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. Author manuscript; available in PMC: 2025 Jul 1.
Published in final edited form as: Neuropsychology. 2024 Apr 11;38(5):475–485. doi: 10.1037/neu0000908

ANHEDONIA REFLECTS AN ENCODING DEFICIT FOR PLEASANT STIMULI IN SCHIZOPHRENIA: EVIDENCE FROM THE EMOTION-INDUCED MEMORY TRADE-OFF EYE TRACKING PARADIGM

Kayla M Whearty 1, Ivan Ruiz 2, Anna R Knippenberg 2, Gregory P Strauss 2,*
PMCID: PMC11864075  NIHMSID: NIHMS2054990  PMID: 38602815

Abstract

OBJECTIVE:

The current study explored the hypothesis that anhedonia reflects an emotional memory impairment for pleasant stimuli, rather than diminished hedonic capacity in individuals with schizophrenia (SZ).

METHOD:

Participants included 30 schizophrenia (SZ) and 30 healthy comparisons subjects (HC) who completed an eye tracking emotion-induced memory trade-off task where contextually relevant pleasant, unpleasant, or neutral items were inserted into the foreground of neutral background scenes. Passive viewing and post-stimulus elaboration blocks were administered to assess differential encoding mechanisms, and immediate and one-week recognition testing phases were completed to assess the effects of delay interval. Participants also made self-reports of positive emotion, negative emotion, and arousal in response to the stimuli.

RESULTS:

Results indicated that SZ experienced stimuli similarly to HC. Both groups demonstrated the typical emotion-induced memory trade-off during the passive viewing and post-stimulus elaboration encoding blocks, as indicated by more hits for emotional than neutral items and fewer hits for backgrounds paired with emotional than neutral items. Eye tracking data also indicated that both groups were more likely to fixate earlier and have longer dwell time on emotional than neutral items. At the one-week delay, the emotion-induced memory trade-off was eliminated in both groups, and SZ showed fewer overall hits across valence conditions. Greater severity of anhedonia was specifically associated with impaired recognition for pleasant stimuli at the immediate recognition phase.

CONCLUSIONS:

Findings suggest that anhedonia in SZ is associated with emotional memory impairment, particularly a deficit in encoding positive stimuli.

Keywords: Negative symptoms, cognition, emotion, encoding, retrieval

Introduction

Anhedonia, traditionally defined as a diminished hedonic capacity (i.e., reduced positive emotion experienced in relation to normatively pleasant stimuli), has been considered a core symptom of schizophrenia (SZ) since the earliest conceptualizations of the disorder (Kraepelin, 1919; Bleuler, 1911). Modern empirical evidence confirms that anhedonia is associated with numerous poor clinical outcomes in SZ (e.g., lower rates of recovery, subjective well-being, risk for illness onset) (Strauss et al., 2010, 2012; Piskulic et al., 2012). Unfortunately, pharmacological and psychosocial treatments have not produced clinically meaningful symptom reduction (Fusar-Poli et al., 2014).

Limited progress in treating anhedonia may be due in part to conceptual confusion regarding the nature of the symptom and its underlying mechanisms (Strauss & Gold, 2012). Evidence for anhedonia primarily comes from clinical symptom interviews indicating that a substantial proportion of SZ are anhedonic (Strauss, 2014). However, modern laboratory-based studies contradict interview-based evidence, indicating that self-reported positive emotion and arousal to pleasant stimuli is comparable between people with SZ and healthy controls (HC) (Cohen & Minor, 2010; Llerena et al., 2012). Neurophysiological and autonomic response to rewards or pleasant stimuli is also intact (Horan et al., 2010, 2012; Ursu et al., 2011; Radua et al, 2015; Kring & Moran, 2008; Kring et al., 2011), and SZ patients report comparable levels of positive emotion to potentially pleasurable events in the context of daily life as measured via ecological momentary assessment (Oorschot et al., 2013; Strauss et al., 2020; Gard et al., 2007).

Collectively, these findings raise an important question: if hedonic capacity is intact in SZ, how are we to understand self-reported anhedonia obtained via clinical interviews? Given that interviews assessing anhedonia rely on retrospective reports of pleasure for timeframes ranging from 1-week to 1 month, it is possible that clinical ratings of anhedonia reflect memory impairment for positive stimuli/events. Indeed, cognitive deficits have long been considered a core clinical feature of SZ (Kraepelin, 1919), and more recently supported by modern meta-analyses of neuropsychological performance (Dickinson et al., 2007; Fioravanti et al., 2005). Further, there has been increasing evidence to suggest that episodic memory deficits in SZ extend to emotional memory (Herbener, 2008). However, findings to date are mixed regarding emotional memory impairment in SZ. Some studies show an emotional memory deficit in SZ (i.e., equivalent memory for emotional and neutral stimuli) (Calev & Edelist, 1993; Hall, Harris, McKirdy, Johnstone, & Lawrie, 2007; Herbener et al., 2007; Koh, Grinker, Marusarz, & Forman, 1981; Koh, Kayton, & Peterson, 1976); however, several others indicate intact emotional memory modulation (Danion, Kazes, Huron, & Karchouni, 2003; Hall et al., 2007; Mathews & Barch, 2004; Sergerie, Armony, Menear, Sutton, & Lepage, 2010; Whalley et al., 2009). There is also inconsistency regarding the nature of emotional memory impairment in SZ, with several studies showing that SZ fail to demonstrate superior memory for pleasant over neutral stimuli, whereas others indicate that the abnormality is characterized by an inversion of the typical positivity effect (i.e., better memory for unpleasant than pleasant) (Herbener, 2008; Dieleman et al., 2013). Inconsistent findings across studies may reflect methodological differences, such as the use of verbal vs. visual stimuli, recall vs. recognition paradigms, and differing lengths of delay interval (Dieleman et al., 2013).

There are a number of questions remaining to be answered regarding emotional memory impairment and anhedonia in SZ. First, it is unclear which aspects of cognition are contributing to emotional memory impairment and whether any of these elements are specifically associated with anhedonia (e.g., attention, encoding, retrieval, retention). Prior studies suggest several plausible candidates. For example, dysfunctional bottom-up and top-down emotion-attention interactions are associated with greater negative symptom severity (Loughland et al., 2002; Streit et al., 1997; Strauss, Llerena, Gold, 2011; Strauss, Catalano, Llerena, Gold, 2013); such deficits could prevent selective encoding of emotional stimuli (i.e., processing incoming information and storing it via acquisition and consolidation). Encoding deficits may also result from factors independent of attention, such as failure to self-initiate encoding strategies (e.g., elaborative rehearsal) that promote consolidation (Paul, Elvevag, Bokat, Weinberger, & Goldberg, 2005; Ragland et al., 2003). Long-term memory deficits have also been identified, with studies indicating an emotional memory impairment in SZ at delay intervals of 24-hours or more; however, results are inconsistent and it is unclear whether there is an association between long-term memory and anhedonia specifically (Dieleman & Roder, 2013; Herbener, 2008). Second, it is unclear whether emotional memory deficits in SZ are selective to pleasant stimuli and if these deficits are greatest in anhedonic patients. Current evidence suggests that greater severity of anhedonia is associated with poorer encoding and retrieval (at immediate and 1-week delays) for positive stimuli specifically (Strauss et al., under review). However, very few studies have sought out to directly test the role of emotional memory in anhedonia, and more research is clearly needed since prior associations between emotional memory and negative symptoms have been found primarily using first-generation rating scales that fail to assess anhedonia (see Supplementary Materials).

The primary aim of the current study was to determine whether clinical ratings of anhedonia in SZ are associated with an emotional memory deficit for pleasant stimuli, and to determine which specific cognitive processes drive the association with anhedonia (i.e., attention, encoding, retrieval, retention). This was accomplished using the emotion-induced memory trade-off paradigm (Steinmetz & Kensinger, 2013), which is capable of isolating multiple cognitive processes that could putatively contribute to anhedonia assessed via clinical interviews. Based on prior studies, it was hypothesized that SZ patients would: 1) report experiencing levels of positive emotion and arousal to pleasant stimuli similarly to controls; 2a) have more hits for unpleasant than neutral items, but no difference in hits between pleasant and neutral items; 2b) fewer hits for backgrounds previously paired with unpleasant items than with neutral items, but no difference between backgrounds previously paired with pleasant and neutral items; 2c) poorer general memory than controls (i.e., fewer hits, more false alarms, and a lower d-prime value) across immediate and long delay phases; 2d) benefit from the post-stimulus elaboration block such that overall, there would be more hits across all emotion categories that were previously viewed in the post-stimulus elaboration block than in the view block; 3) direct less attention to pleasant items in the composite images than controls (i.e., a lower proportion of: fixations spent in the area of interest (AOI), dwell time, and a longer time to first fixation for pleasant items). Patients and controls were expected to attend to unpleasant and neutral items similarly; 4) demonstrate an association between clinically rated anhedonia and poorer memory (hits and d-prime value) and attention (percent of fixations, percent of dwell time, and time of first fixation) for pleasant items at immediate and long-delay testing.

Method

Participants

Data was collected from two participant groups: 1) 30 individuals with DSM-IV-TR diagnoses of SZ and 2) 30 healthy comparison participants (HC). SZ were recruited from local community outpatient mental health centers and identified by their treating psychiatrist for inclusion in the study if they carried a primary SZ diagnosis (American Psychiatric Association, 2000). Clinical diagnosis was confirmed using the Structured Clinical Interview for DSM-IV-TR (SCID), which was informed by consultation with the patient’s treating psychiatrist, other program staff, and review of medical records, when possible. HC participants were recruited from the local community using posted flyers, newspapers advertisements, and electronic advertisements. HC had no current Axis I or II DSM-IV diagnoses as established by the SCID-I and SCID-II (respectively), no family history of psychosis, and none were taking psychotropic medications. All participants were free from lifetime neurological disease and substance use disorders within the last six months. All participants received monetary compensation for their participation. Patient and control groups did not significantly differ on demographic variables known to influence cognitive and affective functioning, including age (range 22–61 years), parental education, sex, and ethnicity (see Table 1).

Table 1.

Participant Demographic and Clinical Characteristics

SZ (n = 30) HC (n = 30) Test Statistic, p-value
Age 41.97(±1.98) 43.83(±2.10) F = 0.42, p = 0.52
Parental Education 13.42(±0.46) 13.33(±0.38) F = 0.02, p = 0.88
% Male 56.7% 63.3% χ 2 = 0.28, p = 0.79
Ethnicity χ 2 = 3.20, p = 0.70
 Caucasian 80.0% 83.3%
 African- American 3.3% 6.7%
 Asian 0.0% 3.3%
 Hispanic/Latino 6.7% 3.3%
 Biracial 6.7% 3.3%
 Other 3.3% 0.0%
BNSS Anhedonia Domain 2.49 (1.56) -- --
BNSS Anhedonia Items 1&2 2.58 (1.58) -- --
BNSS Asociality Domain 2.15 (1.93) -- --
BNSS Avolition Domain 2.63 (1.89) -- --
BNSS Blunted Affect Domain 2.12 (1.88) -- --
BNSS Alogia Domain 1.26 (1.74) -- --
BPRS Positive 3.00 (1.37) -- --
BPRS Disorganized 1.86 (0.75) -- --
BPRS Total 45.67 (9.62) -- --
LOF Total 21.16 (6.43) -- --
% on Antipsychotic 73.3% -- --
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Note. SZ = schizophrenia; CN = healthy comparison

Procedures

All participants signed informed consent for a study approved by the Binghamton University Institutional Review Board. Two testing sessions occurred exactly one week apart. Prior to completing the behavioral and eye-tracking tasks, examiners who were trained to reliability standards, conducted a structured diagnostic interview with patients to complete the SCID and determine Axis I diagnoses. A clinical interview was also completed to assess symptom severity over the past week, after which symptom severity and functional outcome measures were rated, including the Brief Psychiatric Rating Scale (BPRS) (Overall & Gorham, 1962), Brief Negative Symptom Scale (BNSS) (Kirkpatrick et al., 2011), and Level of Function Scale (LOF) (Hawk, 1975). Following clinical interviews, participants completed the immediate phase of the eye-tracking emotional memory test.

One week after having completed the immediate phase, participants returned to the lab to complete session two, which began with an unprompted delayed recognition test. Following the long delay recognition test, subjects completed a behavioral emotional experience task where they made self-reports of emotional experience to pleasant, unpleasant, and neutral composite images. Participants also completed an ecological momentary assessment protocol that was not of focus of the current study (Visser et al., 2018; Strauss et al., 2019).

Measures

The task was modeled after Steinmetz and Kensinger (2013). In this task, participant eye movements are tracked while they view scenes that have a pleasant, unpleasant, or neutral foreground item inserted into a contextually relevant background scene. They are then required to complete recognition memory testing for the item and background stimuli that are presented separately after passively viewing the entire scene, or after passively viewing and completing a post-stimulus elaboration condition designed to promote consolidation that requires answering specific questions about the item and background before recognition memory testing. Following completion of immediate recognition testing, they rate the stimuli for valence and arousal to assess hedonic capacity. One-week later, they also complete recognition memory testing to examine the effects of delay. This paradigm allows for the examination of whether anhedonia reflects reduced hedonic capacity for experiencing pleasant stimuli or a memory deficit that is driven by abnormal attention, encoding, ineffective utilization of memory-enhancing strategies, or retrieval.

The task consisted of 2 phases: Immediate and Delay. In the Immediate phase, there were 2 blocks, View and Post-Stimulus Elaboration, which were always presented sequentially to address the concern that the Post-Stimulus Elaboration block – if presented first – would influence the View block. The Long Delay phase occurred following a one-week delay. A one-week timeframe was chosen because it allows for an assessment of long-term memory and it is consistent with the retrospective reporting timeframe used in the BNSS. An overview of the task and sample trial sequence within each phase/block is presented in Figure 1A.

Figure 1. Trial Diagram.

Figure 1.

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A= Example Trial Diagram: The view block was an incidental encoding session. Each trial began with a fixation target that participants must fixate on for 1000ms (within a 1degree radius of visual angle). A composite stimulus was then presented for 2000ms and participants were asked to attend to the image naturally. In the post-stimulus elaboration block, each trial began with a fixation target, followed by a composite stimulus that participants were asked to study carefully because they will be asked 2 true/false questions immediately after each stimuli. One true/false question pertained to the item in the scene and the other to the background. The immediate recognition condition occurred immediately following the completion of post-stimulus elaboration. This surprise recognition test required participants to indicate (yes/no) whether individually extracted items (pleasant, unpleasant, or neutral stimuli in the foreground) or backgrounds (i.e., the undoctored complex neutral background scene without items inserted) had been previously presented. Delayed recognition occurred a week later and was identical to immediate recognition except different items and backgrounds were used. B= Examples of Task Composite Images and Items/Backgrounds used in Recognition Testing: Examples of (top) composite images with: A. Pleasant, B. Neutral, C. Unpleasant items on neutral backgrounds, (middle) recognition test stimuli which were new and previously seen items and backgrounds presented separately, and (bottom) a neutral and an emotional area of interest (inside circle).

Immediate Phase: View Block.

The view block was an incidental encoding manipulation. Each trial began with a fixation target (black oval with white bulls-eye) that participants had to fixate on for 1000ms within a 1degree radius of visual angle. A composite stimulus (i.e., pleasant, unpleasant, or neutral foreground items on a neutral background) was then presented for 2000ms and participants were asked to attend to the image naturally. A total of three practice trials and 42 experimental trials were administered in random order (14 pleasant, 14 unpleasant, 14 neutral stimuli). Sample pleasant, unpleasant, and neutral composite stimuli are presented in Figure 1B.

Immediate Phase: Post-Stimulus Elaboration Block.

In the post-stimulus elaboration block, each trial began with a fixation target (1000ms), which was followed by a composite stimulus (2000ms) that participants were asked to study carefully. Composite stimuli were followed by two true/false questions that participants were required to answer following stimulus offset. One true/false question pertained to the item in the scene and the other to the background (see Figure 1A for example). True/false questions, taken from Steinmetz and Kensinger (2013), are included in the Supplementary Materials.

Recognition Phase: Immediate.

Immediate recognition testing occurred directly after the post-stimulus elaboration block. The unprompted recognition test required participants to indicate (yes/no) whether individually extracted items (i.e., foreground pleasant, unpleasant, or neutral stimuli that were inserted into the original composite stimuli) or backgrounds (i.e., the undoctored complex neutral background scene without items inserted) had been previously presented. Participants had unlimited time to provide yes/no responses that were recorded via button press. A total of 168 recognition trials were presented: 42 previously studied items (14 pleasant, 14 unpleasant, 14 neutral), 42 previously studied backgrounds (14 previously presented with a pleasant, unpleasant, or neutral item), 42 new items (14 pleasant, 14 unpleasant, 14 neutral), and 42 new backgrounds (all neutral). Half of the previously studied items and backgrounds from each valence category were taken from the view block and half from the post-stimulus elaboration block. Two sets of items and backgrounds were created and these were counterbalanced across novel and previously exposed trials.

Recognition Phase: Long Delay.

The Delay phase occurred exactly one-week after the immediate recognition testing for all subjects. The delayed recognition phase was identical to the immediate recognition phase, except different previously studied images than the ones used at immediate recognition were used and different foils were presented. Specifically, a total of 168 recognition trials were presented: 42 different previously studied items (14 pleasant, 14 unpleasant, 14 neutral), 42 different previously studied backgrounds (14 previously presented with a pleasant, unpleasant, or neutral item), 42 new items (14 pleasant, 14 unpleasant, 14 neutral), and 42 new backgrounds (all neutral). Thus, across the two recognition testing sessions, a total of 336 recognition trials were administered.

Stimuli.

The composite stimuli were 168 complex visual scenes that were created by inserting images of unpleasant, pleasant, or neutral items of objects or people onto neutral background scenes (see Figure 1). All items were incorporated onto backgrounds that would be contextually plausible. Pleasant, unpleasant, and neutral items were similar in size and approximate scene location. Inserted items were taken from the International Affective Picture System (IAPS: Lang, Bradley, & Cuthbert, 1997), photo clip art packages, and online image databases. The 56 pleasant, 56 unpleasant, and 56 neutral items have been shown to differ in valence as expected (unpleasant < neutral < pleasant) and the neutral items were rated as less arousing than the pleasant or unpleasant items; pleasant and unpleasant items did differ from each other in arousal or absolute valence (see Steinmetz & Kensinger, 2013 for details). To control for lower-level visual features, luminance, complexity, root mean square (RMS) contrast, and red, green, and blue color saturation were equated across Phases and Blocks (see Nummenmaa, Hyona, & Calvo, 2006 for procedures). A series of one-way ANOVAs confirmed that composite images did not differ across phases on these variables (see the Supplementary Materials). All composite images were also judged by independent raters to have a similar number of people, buildings, and animals. Each stimulus display measured approximately 700 X 550 pixels, which equals to 16.9 × 13.6 degrees of visual angle at a viewing distance of 70cm and a 1024×768 screen resolution.

Apparatus

Participants were seated 70 cm from a 19” LCD monitor (Dell model P190S) operating at a refresh rate of 60 Hz, with head positioned in a chin-and-forehead rest to reduce motion artifacts. Eye position was recorded monocularly from the right eye at 2000 Hz using an SR Research Eyelink 1000 desk-mounted system with a spatial resolution of 0.1 degrees. A 9-point calibration was used and drift-correction was performed prior to each block.

Clinical, Behavioral, and Eye-Tracking Score Calculations

The average of BNSS items 1 and 2 was calculated to measure anhedonia. These items assess the intensity and frequency of pleasure experienced over the past week in the domains of social, physical, recreational, and work/school activities.

Hedonic capacity was defined as self-reported positive emotion reported in relation to positive stimuli via likert rating on the emotional experience task. Behavioral memory scores of interest for the Immediate and Long Delay recognition testing included: hits (% correct, ie stimuli correctly recognized as being old), false alarms (new pictures incorrectly indicated as being old), and discriminability index. Hits were defined as correct identification of a previously presented image/background. False alarms were defined as incorrect identification of a novel image/background as being previously seen. The discriminability index was calculated using d-prime: Z of hits– Z of false alarms. Each of these calculations was computed separately for each valence (pleasant, unpleasant, and neutral) for items and backgrounds. Encoding was operationalized as hits in the immediate phase (i.e., % correct to a previously presented stimulus).”

Hits for items of pleasant stimuli were selected as the primary dependent variable for testing the key correlations. Pleasant stimuli were used to test the specific hypothesis about anhedonia being correlated with memory for pleasant stimuli specifically. Hits for items were chosen as the primary dependent variable because the “items” (ie foreground images in the composite scene) were pleasant, unpleasant, or neutral (the backgrounds were always neutral in content). The key manipulation in this study was the valence (ie pleasant, unpleasant, or neutral) of the foreground item which allowed the test of differential associations with valenced items. In this paradigm, false alarms are of less interest to testing the anhedonia hypotheses because they are a product of how well participants encode the foreground items (i.e., if they attend to items and encode items, they are more likely to have misses and false alarms on the corresponding backgrounds). Similarly, D-prime which is calculated in relation to both hits and false alarms, is not as pure of a test of memory for the pleasant foreground items (because false alarms are included in its calculation). D-prime and false alarms are of interest primarily as a manipulation check that the task produced the emotion induced memory tradeoff as in Steinmetz et al. (2012)

Data processing was completed via EyeLink DataViewer (SR Research Ltd., Mississauga, ON, Canada). Consecutive fixations with a duration <100ms and within 1° were merged. Remaining fixations <100 ms were removed. Trials with fixation data < 75% of the trial were excluded to remove trials with recording issues or long blinks.

Eye-tracking dependent variables of interest from the View and Post-Stimulus Elaboration Blocks at the Immediate phase included: 1) proportion of fixations spent in the area of interest (AOI) of the composite stimulus (i.e., the foreground item) (a measure of top-down attention), 2) proportion of dwell time in the AOI of the composite stimulus (i.e., total duration of fixations in milliseconds within the AOI) (a measure of top-down attention), 3) time of first fixation within the AOI (i.e., the time in milliseconds at which the first fixation lands within the AOI) (a measure of bottom-up attention). AOI’s were defined as the area of the composite stimulus occupied by the item (pleasant, unpleasant, or neutral). The proportion of total fixations and proportion of dwell time within the AOI reflect the amount of top-down attention allocated to the item vs. the background. Time of first fixation within the AOI reflects the bottom-up capture of attention by the item, with earlier first fixation times reflecting greater bottom-up attraction. Fixations were considered valid if they lasted for a duration of 50ms or longer. As is typically done in scene viewing studies, the first fixation made on each trial was discarded. This is because the first fixation typically represents the position of the last fixation made on the fixation target.

Behavioral Emotional Experience Task

To measure emotional experience and test hypotheses about emotional experience in SZ, participants were asked to rate their in-the-moment emotional experience in response to a subset of composite stimuli to evaluate hypotheses related to state experience of positive emotion, negative emotion, and arousal to the stimuli. Participants provided 3 ratings: 1) How positive the stimulus made them feel; 2) How negative the stimulus made them feel; 3) How calm/excited the stimulus made them feel (i.e., arousal). Self-reports were made using the Self Assessment Manikin (SAM: Lang, 1980) using separate positive (1 not at all to 5 extremely), negative (1 not at all to 5 extremely), and arousal (1 calm to 5 excited) scales. Participants rated their level of positive emotion, negative emotion, and arousal to 2 practice stimuli and 5 pleasant, 5 unpleasant, and 5 neutral composite images (4 from the view block, 4 from the elaboration block, and 7 images comparable to the immediate recognition stimuli in stimulus features that were not included in the main task)”. Participants had unlimited time to provide self-report.

Data Analysis

Hypothesis 1:

Three separate repeated measures ANOVAs (Group x Valence) were conducted to determine if groups differed on self-reported levels of positive emotion, negative emotion, and arousal in response to pleasant, unpleasant, and neutral composite images (see Supplemental Table S1).

Hypothesis 2:

2 Group (SZ, HC) X 2 Block (View, Post-stimulus Elaboration) X 3 Valence (Pleasant, Unpleasant, Neutral) repeated measures ANOVA was conducted separately for items and backgrounds in both the immediate and delay phases using hits as the primary dependent variable (see Table 2). Secondary analyses report results for hits and false alarms and d-prime separately in Supplemental Materials (see Tables S2 and S3).

Table 2.

Behavioral Results for Hits (% Correct)

HC SZ Group Block Valence Block X Valence Group X Valence Group X Block Group X Block X Valence
View Elaboration View Elaboration
U N P U N P U N P U N P
Immediate
 Items 71 (24) 55 (30) 59 (25) 88 (13) 87 (15) 87 (13) 69 (23) 53 (27) 62 (23) 79 (21) 76 (28) 83 (19) F = 0.85, p = 0.36, ηp2 = .01 F = 105.8, p<.001, ηp2 =0.65 F = 9.11, p<.001, ηp2 =0.14 F = 6.67, p = 0.002, ηp2 = 0.10 F = 1.03, p = 0.36, ηp2 =.01 F = 3.36, p = 0.07, ηp2 =0.06 F = 0.04, p = 0.96, ηp2 =.01
 Back. 44 (25) 55 (32) 47 (29) 80 (17) 75 (21) 82 (17) 43 (27) 53 (29) 40 (21) 70 (21) 57 (27) 67 (25) F = 3.26, p = .076, ηp2 =0.05 F = 101, p<.001, ηp2 =0.64 F = 01.8, p = 0.84, ηp2 =0.01 F = 17.26, p <.001, ηp2 = 0.23 F = 0.82, p =0.44, ηp2 = .01 F = 5.13, p = 0.027, ηp2 =0.08 F = 0.74, p = 0.48, ηp2 =0.01
Delay
 Items 62 (22) 61 (23) 64 (27) 66 (25) 49 (25) 59 (23) 42 (28) 41 (27) 28 (26) 51 (29) 41 (27) 51 (28) F = 7.97, p = 0.007, ηp2 =.12 F = 0.01, p = 0.97, ηp2 =.01 F = 5.05, p = 0.008, ηp2 = .08 F = 4.09, p = .019, ηp2 =.07 F = 0.53, p = 0.58, ηp2 =.01 F = 3.43, p = .069, ηp2 =.056 F = 0.26, p = 0.77, ηp2 =0.01
 Back. 56 (25) 52 (30) 55 (29) 44 (24) 41 (26) 36 (28) 39 (25) 35 (22) 41 (29) 40 (27) 39 (20) 32 (22) F = 3.21, p = .08, ηp2 =.05 F = 9.19, p<.001, ηp2 = .14 F = 1.86, p = .16, ηp2 =.03 F = 3.7, = = .028, ηp2 =.06 F = .06, p = .94, ηp2 =.01 F = 7.26, p = .009, ηp2 = .11 F = 0.26, p = 0.77, ηp2 =.01
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Hypothesis 3:

Separate 2 (Group: SZ, HC) X 3 (Valence: Pleasant, Unpleasant, Neutral) repeated measures ANOVAs were conducted to assess whether groups differed on the proportion of dwell time within the AOI of interest during the view block and post-stimulus elaboration blocks. Secondary analyses examined the group x valence interaction for each block using additional exploratory dependent variables (first fixation time, proportion of fixations in AOI) (see Supplemental Materials Table S4).

Hypothesis 4:

Pearson correlations with the Benjamini and Hochberg correction for multiple comparisons were used to determine whether BNSS anhedonia (average of items 1 and 2 that rely on retrospective reports) was associated with: 1) pleasant items hits, false alarms, and d-prime scores at the immediate and delay blocks; 2) proportion of dwell time within the AOI of interest for pleasant items during the view and post-stimulus elaboration blocks (see Table 4). Secondary/exploratory correlations were conducted to partial out depression and explore association between anhedonia and additional variables (basic neuropsychological functioning, unpleasant and neutral valence memory scores, additional eye tracking variables).

Table 4.

Correlations Between Anhedonia and Primary Task Variables for Pleasant Stimuli

r p-value
Immediate Recognition View Condition Item Hits Pleasant Stimuli −.40 .02
Immediate Recognition Elaboration Condition Item Hits Pleasant Stimuli −.38 .03
Delay Recognition View Condition Item Hits Pleasant Stimuli −.15 .42
Delay Recognition Elaboration Condition Item Hits Pleasant Stimuli −.03 .87
% Dwell Time View Condition Pleasant Stimuli .23 .23
% Dwell Time Elaboration Condition Pleasant Stimuli −.12 .52
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Results

Hypothesis 1

On the emotional experience task, SZ and HC reported experiencing similar levels of positive emotion, negative emotion, and arousal to the pleasant, unpleasant, and neutral stimuli (see Table S1). Magnitude of emotional response to pleasant and unpleasant stimuli was moderate in both groups, as expected.

Hypothesis 2

Analyses of hits and false positives indicated that the task was valid, producing similar effects of Steinmetz and Kensinger (2013) in both groups. Specifically, selective item memory and the emotion induced memory tradeoff occurred – there were: 1) more hits for emotional than neutral items (see Table 2), 2) less hits for backgrounds previously paired with emotional than neutral items (see Table 2); 3) more false alarms for pleasant stimuli, followed by unpleasant, then neutral stimuli (see Table S2); 4) a higher number of false alarms for backgrounds than items (see Table S2).

Hypothesis 3

For the View Block, the Valence X Group interaction was significant, as was the main effect of Valence, with the longest dwell time occurring for pleasant items, followed by neutral, then unpleasant. The between subjects effect of group was nonsignificant. Follow-up analyses indicated that for patients, the longest item dwell time was for pleasant items, then unpleasant, and then neutral. For controls, the longest item dwell time was for pleasant items, then neutral, and then unpleasant.

For the Post-Stimulus Elaboration Block, the 2 (Group: SZ, HC) X 3 (Valence: Pleasant, Unpleasant, Neutral) repeated measures ANOVA was conducted to assess whether groups differed on the proportion of dwell time within the AOI of interest during the post-stimulus elaboration block. The main effect of Valence was significant, as was the between subjects effect of group. The Valence X Group interaction was nonsignificant. The proportion of dwell time was longest for pleasant items, followed by neutral, and then unpleasant items, and patients had longer dwell time than controls across valence categories.

Hypothesis 4

Primary correlations used to test hypothesis 4 indicated that in the immediate recognition phase, greater severity of BNSS anhedonia was associated with fewer hits for items for pleasant stimuli in both the view and post-stimulus elaboration blocks (see Table 4). These correlations survived the Benjamini and Hochberg correction for multiple comparisons and remained significant after partialing out the effects of BPRS depression scores (see Table S10). Associations between these variables and other experiential negative symptoms, asociality and avolition, were nonsignificant. At delayed recognition, there was no significant association between anehdonia and hits for pleasant stimuli (see Table 4). Anhedonia was also not significantly associated with eye tracking variables in the view or post-stimulus elaboration blocks (see Table 4).

Secondary correlational analyses conducted for exploratory purposes indicated that anhedonia was not significantly associated with: 1) hits for neutral and unpleasant stimuli at immediate or delay testing; 2) d-prime for pleasant, unpleasant, or neutral stimuli at immediate or delayed recognition; 3) first fixation time or % AOI fixation for pleasant, unpleasant, or neutral stimuli in the view or elaboration conditions (see Tables S11). Antipsychotic use was also not associated with task variables.

Discussion

The current study was designed to tease apart the mechanisms underlying the association between anhedonia and poor memory for pleasant stimuli in SZ. Specifically, we examined whether the association was due to reduced hedonic capacity for experiencing pleasant stimuli, attention, encoding, effective utilization of memory-enhancing strategies, or retrieval. The results indicated that patients reported experiencing the stimuli similarly to controls and there was no evidence that patients exhibited a reduced hedonic capacity for pleasant stimuli.

The primary deficit that was associated with anhedonia was fewer hits for pleasant stimuli at the immediate recognition phase. Importantly, this deficit existed in the context of intact attention. This finding suggests that the problem is more due to encoding than attention. Even though people with schizophrenia attend to the items within the pleasant scene, this information fails to be effectively encoded in a way that can later be accessed. However, much like controls, providing patients with a memory-enhancing strategy such as post-stimulus elaboration, significantly enhanced encoding for emotional information. This effect is comparable to what was observed in non-emotional tasks (Paul et al., 2005), which have indicated that people with SZ benefit from prompts aimed at enhancing memory. In fact, our results indicate that SZ patients benefit from the post-stimulus elaboration strategy to a greater extent than HC. However, even though these benefits are significant, they are not long lasting. The one-week delay period eliminated the emotion-induced memory trade-off effect, lowering hits and increasing false alarms comparably in both groups. Anhedonia was not associated with performance in the delay recognition phase – potentially due to reduced variance and floor effects.

The results of the current study implicate poor encoding of pleasant stimuli as a primary mechanism involved with ratings of anhedonia obtained using standard retrospective clinical interviews. Essentially, even though patients attend to and experience stimuli normally, they may not encode or organize them into memory in a way that they can later be efficiently retrieved after a significant delay. At first glance, these findings appear inconsistent with some prior studies indicating that SZ patients with negative symptoms fail to display a bottom-up competitive advantage for pleasant stimuli (Strauss et al., 2013). However, the differences among methods used in these studies may be informative regarding the nature of emotional information processing deficits observed in SZ. Specifically, the emotional attentional blink paradigm used in Strauss et al. (2013) manipulates temporal (rather than spatial) dynamics and relies on both attentional orienting and working memory updating processes. Since other studies using eye tracking that also rely on spatial manipulations have also observed intact bottom-up attention to emotional stimuli in SZ, it is possible that some prior findings more accurately reflect failures in encoding (i.e., due to problems with consolidation and working memory updating), rather than bottom-up attention per se.

Regarding findings on memory, the current results generally support prior studies showing that memory is effectively modulated by emotional stimuli at the group level (Herbener, 2008; Dielman, 2013), but clarify that individuals with clinically elevated anhedonia may have a distinct profile of impairment characterized by poor encoding for pleasant stimuli. Some prior studies (Culbreth et al., 2020; Hall, 2007; Matthews & Barch, 2004), but not the majority (Herbener, 2009; Herbener et al., 2007; Kline, 1992; Neuman, 2007ab; Harvey, 2009), report an association between negative symptoms and emotional memory. Inconsistencies among prior studies may reflect the differences among stimulus types (e.g., words vs pictures), stimulus modality (verbal vs visual), memory processes assessed (encoding vs long-term memory), and negative symptom measures used (the majority of prior studies not finding an association have used older negative symptom measures that do not assess anhedonia or do not assess it using modern conceptualizations). Additionally, in the current study, anhedonia was not significantly associated with standard neuropsychological measures of memory, even though it was significantly associated with emotional memory. However, prior studies provide somewhat consistent evidence for an association between anhedonia and standard (non-emotional) neuropsychological tests of memory at a small effect size (see Strauss & Gold, 2012) that is consistent with results observed here, suggesting roles for both general and emotion-specific memory processes in clinically rated anhedonia. Additional studies are needed that use neuroimaging and emotional memory paradigms to determine whether encoding deficits associated with anhedonia reflect general or emotion-specific deficits. This could be accomplished by examining differential patterns of activation associated with anhedonia across emotional and neutral task conditions. Cahill and McGaugh (1998) have demonstrated that superior memory for emotional stimuli results from increased amygdala activity at encoding, which initiates a cascade of neurobiological processes that further support transfer of information to long-term memory. If future studies suggest differential associations between anhedonia and activation of emotional regions, such as the amygdala, above and beyond pre-frontal regions required for encoding more generally, this would support an emotion-specific anhedonia deficit.

Certain limitations should be considered. First, the study included chronic outpatients and results might differ among those at earlier stages of illness. Second, only one emotional memory paradigm was administered. Although comprehensive in the multiple cognitive processes it assesses, the emotion induced memory-trade-off paradigm still could not cover all relevant variables known to produce inconsistency in prior studies (e.g., verbal vs visual stimuli, delay interval length). Third, a 1-week delay interval was used to most closely map onto the length of retrospective reports used in clinical trials; however, only obtaining immediate and 1-week delay recognition prevented the evaluation of a forgetting curve. When long-term memory for emotional stimuli becomes aberrant in SZ is therefore still unclear. Fourth, we were unable to validly quantify the role of secondary negative symptom sources (e.g., depression) in the link between emotional memory and anhedonia; although partial correlations remained significant after partialing out the effects of depression, fully investigating this effect will be an important future direction. Finally, findings were purely behavioral. Neurobiological mechanisms should be examined in future studies.

Despite these limitations, findings of the current study have implications for conceptualizing and treating anhedonia. Results indicated that individuals with SZ did not show a hedonic deficit to pleasant stimuli; however, patients with more severe anhedonia showed a deficit in encoding pleasant stimuli. These findings are consistent with recent proposals that anhedonia rated on retrospective clinical interviews may reflect more of a cognitive deficit than an experiential abnormality. If replicated in future studies, these findings suggest that treatments for anhedonia that are aimed solely at augmenting emotional experience may not be optimal. (Favrod et al., 2015; Johnson et al., 2011; Meyer, Johnson, Parks, Iwanski, & Penn, 2012; Nguyen et al., 2016). Psychosocial interventions may benefit from targeting encoding mechanisms specifically.

Supplementary Material

supplemental material

Table 3.

Percentage Dwell Time in Emotional Areas of Interest

% Dwell Time HC SZ
U N P U N P Group Valence Group X Valence
View Block 62% (13%) 64% (12%) 67% (13%) 58% (13%) 57% (13%) 66% (13%) F = 1.90, p = 0.17, ηp2 =0.03 F = 23.9, p<.001, ηp2 =0.29 F = 4.67, p = .01, ηp2 =.08
Elaboration Block 50% (08%) 56% (08%) 59% (10%) 56% (09%) 58% (08%) 65% (09%) F = 4.87, p = .03, ηp2 =.08 F = 35.4, p<.001, ηp2 =0.38 F = 2.07, p =0.13, ηp2 =0.04
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Key Points.

Question:

Is anhedonia associated with an emotional memory impairment in schizophrenia?

Findings:

Anhedonia was selectively associated with a deficit in encoding pleasant stimuli; however, it was not associated with impairments in attention or long-term memory for pleasant stimuli.

Importance:

Clinically rated anhedonia, which relies on retrospective reports of pleasure, is associated with impaired encoding for positive information in schizophrenia (i.e., a cognitive deficit)

Next Steps:

Additional research examining the role of emotional memory in anhedonia in schizophrenia is needed using neuroimaging to identify neural substrates of the encoding deficit reported here; cognitive training interventions focused on encoding may be beneficial for improving clinical outcome if findings are consistently replicated.

Acknowledgments

Research supported in part by U.S. National Institutes of Mental Health Grant K23MH092530 and an Interdisciplinary Collaboration grant from the State University of New York to Gregory P. Strauss. We are indebted to the subjects who participated in the study and staff in the Translational Affective Neuroscience Laboratory, particularly Katherine Frost and Elizabeth Dickinson

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