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Review 31 (2011) 440–448

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Clinical Psychology Review

The state-trait disjunction of anhedonia in : Potential affective, cognitive and social-based mechanisms

Alex S. Cohen ⁎, Gina M. Najolia, Laura A. Brown, Kyle S. Minor

Department of Psychology, Louisiana State University, United States article info abstract

Article history: Dysfunctions in affective experience reflect a pernicious feature of schizophrenia-spectrum pathology that are Received 22 March 2010 largely intractable under current treatment regimens. Of note, individuals with schizophrenia show robust Accepted 4 November 2010 and marked deficits in the experience of when assessed using “trait” measures of affect (i.e., trait Available online 12 November 2010 questionnaires and clinical interview), but fail to demonstrate this anhedonia “in the moment” using controlled laboratory mood-induction procedures. The reasons for this disjunction are unclear, but the last Keywords: decade has seen a number of recent studies tackling this issue. We conduct a comprehensive review of this Schizophrenia fi Emotion literature here. Five different explanations for this state-trait disjunction are identi ed: 1) anticipatory Affect hedonic experience deficit, 2) affective regulation deficit, 3) encoding-retrieval deficit, 4) representational Anhedonia deficit and 5) social-specificdeficit theories. Our present article reviews each of these theories, placing them State in context of the larger affective and cognitive neuroscience literatures when appropriate. Additionally, Trait practical recommendations for future studies examining affective dysfunction within the schizophrenia- Negative spectrum are discussed. Mood © 2010 Elsevier Ltd. All rights reserved. Review

Contents

1. Introduction ...... 440 2. Specific affective deficit: Anticipatory hedonic experience ...... 441 3. Affective regulation deficit...... 442 4. Encoding-retrieval deficit...... 442 5. Representational deficit...... 443 6. Social-specific hedonic deficit...... 444 7. Summary and integration ...... 446 References ...... 446

1. Introduction empirical study of anhedonia in schizophrenia has provided incon- sistent support for this notion. On the one hand, patients generally Dysfunctions in affective experience are a critical aspect of report attenuated experience of pleasant emotions on self-report schizophrenia-spectrum pathology as they often precede illness trait-based instruments of hedonic experience (Berenbaum & Fujita, onset (Kwapil, 1998; Walker & Lewine, 1990) and are associated 1994; Horan, Blanchard, Clark, & Green, 2008). Moreover, trained with a range of social and occupational impairments (Blanchard, experts rate individuals with schizophrenia as having abnormally Mueser, & Bellack, 1998; Cohen et al., 2005). Of note, anhedonia, high levels of anhedonia using interview-rated instruments, typically defined as an inability to experience pleasant emotions, is postulated spanning week-long epochs (e.g., Blanchard & Cohen, 2006; Sayers, to be a core symptom reflecting a latent vulnerability marker of the Curran, & Mueser, 1996). However, examinations of state emotions disorder (Docherty & Sponheim, 2008; Meehl, 1962). Nonetheless, under controlled laboratory conditions have revealed that individuals with schizophrenia report experiencing normal levels of pleasant emotions while processing a broad range of stimuli (Cohen & Minor, ⁎ Corresponding author. Department of Psychology, Louisiana State University, 236 Audubon Hall, Baton Rouge, LA 70808, United States. Tel.: +1 225 578 7017. 2010; Kring & Moran, 2008). Similarly, when individuals with E-mail address: [email protected] (A.S. Cohen). schizophrenia are asked about their state emotions while navigating

0272-7358/$ – see front matter © 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.cpr.2010.11.001 A.S. Cohen et al. / Clinical Psychology Review 31 (2011) 440–448 441 through their natural environments as part of Experience Sampling assessed using very specific affect probes (e.g., “How do you feel at this Methodologies, they report relatively normal pleasant emotional exact moment?”) following laboratory mood-induction procedures. In reactions (Myin-Germeys, Delespaul, & deVries, 2000; Myin-Germeys, order to directly compare anticipatory and consummatory pleasure, van Os, Schwartz, Stone, & Delespaul, 2001). Thus, there appears to be similar assessment domains and methods should be employed. Two a disjunction between trait and state report of emotional experience recent lines of research have addressed this issue and offer in schizophrenia. The mechanism underlying this disjunction is preliminary support for the notion that anticipatory but not unknown. We believe that understanding this issue may offer consummatory systems are affected in schizophrenia. Gard, Gard, important insights into the nature of schizophrenia pathology. The Kring, and John (2006) developed the Temporal Experience of present paper examines five separate theories that could explain the Pleasure Scale (TEPS), a brief self-report questionnaire designed to state-trait disjunction. While these theories are not necessarily separately assess anticipatory and consummatory pleasure experi- mutually exclusive, they do differ in term of the larger affective, ence. The TEPS consists of ten anticipatory (“I get so excited the night cognitive and social literatures that they draw from. These five before a major holiday I can hardly sleep.”) and eight consummatory theories are: 1) anticipatory hedonic experience theory, 2) affective (“I enjoy taking a deep breath of fresh air when I walk outside.”) items, regulation deficit theory, 3) encoding-retrieval deficit theory, 4) with good internal reliability for the total scale, acceptable reliability representational deficit theory, and 5) social-specificdeficit theory. for the subscales, good test–retest reliability and both convergent and The literature from a broad range of schizophrenia-spectrum studies divergent validity. Gard et al. (2007) reported that patients with is examined here and grounded in the larger affective and cognitive schizophrenia versus non-psychiatric controls reported abnormally neuroscience literatures when appropriate. low anticipatory, but not consummatory, pleasure. In terms of divergent validity, the anticipatory, but not the consummatory, 2. Specific affective deficit: Anticipatory hedonic experience subscale scores were significantly correlated with scores from another widely used and validated self report measure of social anhedonia One theory offered to explain the discrepancy between state and (i.e., the Revised Social Anhedonia Scale; Eckblad et al., 1982), and trait emotion is that schizophrenia patients possess a relatively scores from an interviewer-rated instrument (i.e., the Schedule for the specificdeficit in affective processes that compromises their ability to Assessment of Negative Symptoms; Andreasen, 1983). accurately forecast affective experiences. In contrast, patients' ability Perhaps the most compelling evidence supporting specific antic- to experience affect “in the moment” is intact. As discussed below, ipatory affective deficit hypothesis comes from an Experience there is solid support for the notion that “anticipatory” hedonic Sampling Methodology study examining differences in self-reported systems, involving the ability to predict the future experience of anticipatory and consummatory pleasure in individuals with schizo- pleasure, are distinct from “consummatory” hedonic systems, involv- phrenia (Gard et al., 2007). During the study, participants were paged ing experience of stimuli “on-line” (Gard, Kring, Gard, Horan, & Green, seven times throughout the day for one week and asked to 2007; Horan et al., 2008). It follows that when individuals with record what they were doing and how much they were enjoying it schizophrenia are asked to evaluate their reactions to potential events (i.e., consummatory pleasure). They were also asked to record what as part of a questionnaire or a clinical interview – presumably they were looking forward to doing and how much pleasure they activating “anticipatory” hedonic neurocircuitry, they consistently anticipated experiencing during the activity. Overall, patients report experiencing diminished hedonic reactions. However, when reported anticipating less pleasure from future activities than consummatory systems are activated by “in the moment” experience controls at a trend level (p=0.06), but there was no difference in of stimuli, hedonic experience is normal. consummatory ratings. This finding is impressive in light of the small There is considerable support from neuroscience more generally sample size employed as there were only fifteen patients and twelve that anticipatory and consummatory pleasure systems are neurobio- controls. An interesting pattern emerged when future activities were logically distinct. Distinct neural pathways have been identified categorized as “goal-directed” (e.g., making dinner and doing an related to the experience of “wanting” (analogous to anticipatory errand) or “non-goal directed” (e.g., eating dinner and watching TV) pleasure) vs. “liking” (analogous to consummatory pleasure) (Ber- activities. Consummatory pleasure was not significantly different for ridge & Robinson, 1998, 2003; Gard et al., 2007; Knutson, Adams, either category. Individuals with schizophrenia, however, looked Fong, & Hommer, 2001). For example, drug and dependence in forward to and engaged in goal-directed activities significantly less humans has been shown to persist even after the separate experience often and anticipated receiving significantly less pleasure from goal- of pleasure during use is diminished (Berrridge, 2007; Berridge & directed activities compared to controls; group differences in Robinson, 1995; Hobbs, Remington, & Glautier, 2005; Lambert, anticipatory pleasure for non-goal directed activities were nonsignif- McLeod, & Schenk, 2006). Further support is seen at a neurobiological icant. In summary, individuals with schizophrenia consistently level, as has shown to be strongly linked to anticipatory predicted experiencing abnormally low levels of pleasant emotions rather than consummatory pleasure (Berrridge, 2007; Berridge & for goal-directed activities, but reported normal experiences on “in Robinson, 1998). In contrast, the experience of consummatory the moment” assessments. pleasure has been more strongly linked to the and While the specific anticipatory affective deficit hypothesis is systems (Berridge & Robinson, 1998;2003; Schultz, 2002; Wise, particularly promising, there are several issues to contend with. 2002). Given that dopaminergic abnormalities are considered central First, some have raised suspicions that deficits in anticipatory pleasure to core schizophrenia pathology (Kapur & Mamo, 2003; Stanislaw & are iatrogenic consequences of medication rather than Carson, 2004), arguably more so than either opioid or serotonin idiopathic features of the disorder. Gard et al. (2007) argue that this is abnormalities (Abi-Dargham, 2007; Laurelle et al., 2000; Peckys & not the case, as the decreased activity in brain regions associated with Hurd, 2001), it stands to reason that anticipatory pleasure would be reward anticipation (e.g., ventral ) are also evident in affected in patients. unmedicated patients presented with reward-indicating cues (Juckel A challenge for this line of research concerns the lack of validated et al., 2006). Second, anticipatory and consummatory pleasure assessments for distinguishing between anticipatory and consumma- assessments are particularly difficult to match, especially for a tory pleasure that can readily be applied to schizophrenia populations. schizophrenia population who may suffer from a host of cognitive As noted above, anticipatory pleasure abilities have been assessed difficulties. This is a particular concern for questionnaire-based from responses to self-report questionnaire and interview items assessments which may employ complicated phrasings or may assessing a broad range of potential experiences (e.g., “How do you require high levels of abstraction to “affectively forecast” pleasure generally feel?”) whereas consummatory pleasure abilities have been states in the future. All items on the TEPS (anticipatory and 442 A.S. Cohen et al. / Clinical Psychology Review 31 (2011) 440–448 consummatory) require some level of abstraction as participants must magnitude (mean weighted Cohen's d=0.72 and 0.64 for pleasant consider their hedonic experiences in the absence of immediately and neutral stimuli respectively) and in consistency across studies – affectively-relevant stimuli, and both subscales may tap into similar each of the eleven studies included in this analysis reported processes that may reflective at some level of anticipatory mecha- differences between controls and patients at the medium effect size nisms. Third, it is important to note that hedonic experience is a broad level or greater (range of Cohen's d values=0.51–1.31). These results construct encompassing a wide range of social, physical and support the notion that increased negative affectivity, as opposed to intellectual domains. The TEPS items contain exclusively physical decreased positive affectivity (i.e., anhedonia) is the chief domain in stimuli and there is research to suggest that hedonic dysfunction in which affective experience is disrupted in schizophrenia. the social domain is particularly relevant to schizophrenia spectrum Another study of state emotion warrants mention here, as it disorders (see section six). employed a different approach to understanding emotional reactions than explicit self-report. Cohen, St-Hillaire, Aakre, and Docherty 3. Affective regulation deficit (2009b) examined lexical expression of individuals during a labora- tory narrative exercise. Specifically, participants were asked to discuss Another possibility is that the state-trait disjunction reflects a positive, negative, and neutral memories from their lives. The speech global affective regulation deficit. Affective regulation deficits reflect a was transcribed and analyzed using Pennebaker's Lexical and Inquiry variety of deliberate and automatic strategies for downregulating Word Count system, which has been used to understand emotion unpleasant emotional states and enhancing pleasant ones (Gross, across a range of psychological issues (e.g., deceptive language, Bond 1998; Westen, Muderrisoglu, Fowler, Shelder, & Koren, 1997). & Lee, 2005; suicidality, Handelman & Lester, 2007; , Affective regulation is vital to psychological well-being. For example, Vanheule, Desmet, & Meganck, 2000; trauma adjustment, Beaudreau, difficulty in affect regulation is a core feature of various disorders and 2007), and has been validated as a method for measuring verbal harmful behavior, such as Borderline Personality Disorder (Conklin, expression of emotion (Bantam & Owen, 2009; Kahn, Tobin, Massey, & Bradley, & Westen, 2006), suicidal behavior (Yen, Zlotnick, & Costello, Anderson, 2007). Patients with schizophrenia who were rated as 2002; Zlotnick, Donaldson, Spirito, & Pearlstein, 1997), posttraumatic being clinically anhedonic based on available information (self-report stress (Van der Kolk et al., 1996), and vulnerability to marijuana use and medical records), patients with schizophrenia but without problems (Simons & Carey, 2002). We posit here that individuals with anhedonia, and controls were compared on the percentage of total schizophrenia may show a specificdeficit in the ability to attenuate words that had a pleasant (e.g., love and cheer) and unpleasant unpleasant emotional states, and this, in turn, contaminates the (e.g., kill and bad) valence. Patients with anhedonia showed a experience of pleasant states. dramatic increase in words expressing unpleasant emotion when There is good reason to think that an affective regulation deficit instructed to discuss pleasurable memories from their lives compared explains the state-trait disjunction in schizophrenia. The neural to the other groups, but no corresponding decrease in positive structures thought to be involved in affective regulation processes emotions. These results further the notion that anhedonia, at least as it include the prefrontal and anterior cingulate cortex (ACC) regions is measured using interview-rated instruments, reflects poor regula- (Kross, Davidson, Weber, & Ochsner, 2009; Ochsner, Bunge, Gross, & tion of negative affect rather than a deficit in positive affect. Gabrieli, 2002). One function these structures appear to serve involves More support for the affective regulation deficit theory comes from down-regulating negative affectivity arising from limbic region a study by Trémeau et al. (2009) examining subjective ratings to a structures, notably the (Davidson, 2003; Ochsner et al., variety of positive and negative stimuli presented in the laboratory. 2002). Direct connections are well documented between these three Individuals with schizophrenia reported experiencing abnormally structures, and a number of imaging studies have also demonstrated high levels of conflicting emotions – more negative emotions to that neural activity in prefrontal and ACC regions mediate amgygdala positive stimuli and more positive emotions to negative stimuli. activity (Kross et al., 2009). Dysfunction in each of these brain regions Moreover, self-reported trait anhedonia was significantly associated is prominent in individuals with schizophrenia, notably aberrant ACC with state negative ratings in the presence of pleasant stimuli, and this (Heckers et al., 2004), prefrontal (Barch, Sheline, Csernansky, & relationship was more robust than the relationship between self- Snyder, 2003) and increased “resting” amygdala (Taylor, Phan, reported trait anhedonia and state pleasant ratings. It is also Britton, & Liberzon, 2005) activity relative to non-psychiatric controls. noteworthy that abnormally high negative emotion evoked from Further, conflict monitoring and working memory, abilities depen- positive stimuli was associated with a range of clinical variables, such dent on intact ACC and prefrontal cortical functions (Ko et al., 2009), as increased global illness severity and poorer overall functional life are impaired in schizophrenia patients compared to controls (Kim et skills. al., 2009). Affective regulation deficit theory posits that decreased frontal resources contributes to difficulty regulating limbic over- 4. Encoding-retrieval deficit activity in schizophrenia (Cohen & Minor, 2010; Kerns & Becker, 2008). The encoding-retrieval deficit is the third possible explanation for If an affective regulation theory were a valid explanation for the state-trait disjunction in schizophrenia. It may be the case that “state-trait” disjunction in schizophrenia, we would expect that affective experience is not directly affected in individuals with individuals with schizophrenia would not only report abnormally schizophrenia, but that encoding or recall dysfunction leads to high levels of negative emotion on trait questionnaires, but also on inaccurate representations of these experiences when questionnaires assessments of state emotion during laboratory mood induction. or clinical interviews are administered. For example, an individual Negative emotion, unchecked by ACC and prefrontal regulatory confronted with the statement “I like playing with and petting soft mechanisms, would be prominent in reports of trait affectivity and little kittens or puppies” (from the Revised Physical Anhedonia Scale; when processing stimuli “in the moment.” This is exactly what is seen. Chapman & Chapman, 1978), may have difficulty recalling petting a A recent meta-analysis of studies examining emotional reactivity of kitten or puppy before, how often they have played with a kitten or schizophrenia patients during laboratory assessments (Cohen & puppy, and what the context surrounding these events was. This Minor, 2010) found that although patients did not differ from control hypothesis is attractive in light of findings that memory deficits are subjects in subjective pleasant affective reactions to evocative stimuli pronounced in individuals with schizophrenia (Bilder et al., 2000; (as discussed above), they reported abnormally strong co-occurring Danion, Rizzo, & Bruant, 1999; Gold, Randolph, Carpenter, Goldberg, & unpleasant affective reactions. This effect was seen in response to a Weinberger, 1992; Huron et al., 1995), particularly for memories wide range of positive and neutral stimuli and was striking in pertaining to autobiographical events (Neumann, Blairy, Lecompte, & A.S. Cohen et al. / Clinical Psychology Review 31 (2011) 440–448 443

Philippot, 2007). Furthermore, two comprehensive reviews of yet, data supporting abnormal memory performance for affective neurocognitive deficits in schizophrenia have concluded that verbal stimuli in schizophrenia are mixed. To our knowledge, nine studies memory deficits reflect the most disrupted of neurocognitive have examined emotional memory performance in patients with functions in schizophrenia (Green, 1996; Heinrichs & Zakzanis, 1998). schizophrenia, with five of the nine reporting some degree of In considering this theory, one may ask why encoding or recall emotion-specific abnormality (Calev & Edelist, 1993; Hall, Harris, deficits would result in patients with schizophrenia consistently McKirdy, Johnstone, & Lawrie, 2007; Herbener, Rosen, Khine, & showing, in the absence of a stable memory representation, a Sweeney, 2007; Koh, Grinker, Marusarz, & Forman, 1981; Neumann et “negativistic bias.” If they truly did not remember past experiences, al., 2007) and four reporting no abnormalities at all (Danion, Kazes, one might conclude that their responses should reflect a more random Huron, & Karchouni, 2003; Horan, Green, Kring, & Nuechterlein, 2006; response style. There are two potential answers to this concern. First, Koh, Kayton, & Peterson, 1976; Mathews & Barch, 2004). it could be the case that patients' responses are more random than When evaluating this literature, there are two important issues. controls but their summary scores on tests of hedonic experience are The first is whether memory dysfunctions occur as a function of significantly lower than controls who are more accurate when pleasant stimuli, unpleasant stimuli, or both. This issue is unclear predicting their hedonic experiences. For example, on a “true/false” because of inconsistency across studies. Three studies report that, format questionnaire assessing hedonic experience (e.g., Revised compared to controls, individuals with schizophrenia have signifi- Social Anhedonia Scale), individuals with random response style cantly poorer memory for pleasant stimuli (Calev & Edelist, 1993; would presumably score close to 50%, which is much higher than Herbener et al., 2007; Koh et al., 1981), one study reports poorer control participants, who endorse approximately 15–20% of items memory for unpleasant stimuli (Neumann et al., 2007) and one study assessing schizotypal traits as true (Chapman, Chapman, & Raulin, reports poor memory for both (Hall et al., 2007). Thus, memory 1976). However, evidence against a random response style in patients dysfunctions for pleasant stimuli have only been found in four of the concerns high test-retest reliability and internal consistency on self- nine studies to date. The second issue concerns the amount of time report trait questionnaires in patients with schizophrenia (e.g., between encoding of stimuli and recall (Herbener, 2008), as it may be Blanchard et al., 1998; Herbener & Harrow, 2002). The second the case that the delay between presentation leads to abnormal possibility is that patients show a more global negative bias that colors decaying of affective memory traces. All of the null-finding studies their interpretation of item content. In the absence of compelling listed above employed short encoding/recall delays - two studies had memories to guide one's response to a question assessing hedonic no delay (Koh et al., 1976; Mathews & Barch, 2004), one had a fifteen experience, patients' natural tendency is to respond with a negativ- minute delay (Danion et al., 2003), and one had a four hour delay istic bias. Although to our knowledge this hypothesis remains (Horan et al., 2006). In contrast, four of the five studies finding untested, individuals with schizophrenia have shown a host of affective memory deficits had recall delays of at least one day, ranging cognitive biases when interpreting stimuli. In addition to the negative from 24 h (Herbener et al., 2007; Neumann et al., 2007)to48h(Calev bias reviewed in Section 2 of this paper, there is evidence that some & Edelist, 1993) to three weeks (Hall et al., 2007). In fact, in the two individuals with schizophrenia (Cohen, Nienow, Dinzeo, & Docherty, studies where both immediate and delayed recall were examined 2009; Kohler et al., 2003) or those at high risk for schizophrenia (Calev & Edelist, 1993; Hall et al., 2007), individuals with schizophre- (Brown & Cohen, 2010) show a negative bias when interpreting facial nia did not differ in immediate recognition of emotional stimuli, but expressions or an attentional bias toward threatening facial expres- were significantly worse at recalling emotional stimuli after delay. sions (Green, Williams, & Davidson, 2001). There is also evidence for From these studies, it appears that individuals with schizophrenia other cognitive biases in individuals with schizophrenia such as might not show abnormal memory for valenced stimuli after a brief attribution of negative events to external causes (Aakre, Seghers, St- delay period. With more extended delay, they appear to show Hilaire, & Docherty, 2009) or jumping to conclusions (Moritz & difficulties with integrating or retrieving affective memories. Herb- Woodward, 2005). ener et al. (2007) have proposed that anhedonia may result from an When discussing memory for affective stimuli, it is important to inability to consolidate experiences into long-term memory—a notion note that healthy adults show an enhanced ability to recall that nicely fits the aforementioned data. emotionally valenced versus neutral/non-valenced stimuli (Bradley & Mathews, 1983, 1988; Canli, Zhao, Desmond, Glover, & Gabrieli, 5. Representational deficit 1999; Dolcos, LaBar, & Cabeza, 2004; Fiedler, Pampe, & Scherf, 1986; Hamann, 2001; Rusting, 1998). This bias for emotionally valenced The fourth hypothesis explaining the state-trait disjunction in information may be partially explained by the memory modulation schizophrenia involves a specificdeficit in the ability to mentally hypothesis (McGaugh, 2004), which posits that the amygdala plays an represent the values of stimuli. The representational deficit theory, important role in the encoding and recall of emotional experiences. advanced by Gold and colleagues (Gold, Waltz, Prentice, Morris, & Supporting this hypothesis, healthy adults who exhibit increased Heerey, 2008), purports that patients' ability to experience in-the- activation of the amygdala when encoding emotionally valenced moment pleasure is not directly compromised, but their ability to stimuli have demonstrated enhanced recall of this information later develop a stable mental representation pairing valence and a specific (Canli, Zhao, Brewer, Gabrieli, & Cahill, 2000; Kensinger & Corkin, stimulus is impaired. This in turn attenuates motivation to seek out 2004). In contrast, evidence suggests that patients with schizophrenia the activity or stimulus in the future. Therefore, state experience is have decreased amygdala volume (Lawrie & Abukmeil, 1998; Wright preserved, but in the absence of the stimuli, the hedonic properties of et al., 2000) and exhibit less amygdala activation when encoding the stimuli are lost. While there is potential overlap between this emotionally valenced stimuli (Takahashi et al., 2004; Taylor, Liberzon, theory and the encoding-retrieval deficit discussed above, the Decker, & Koeppe, 2002), although delayed memory for these stimuli representational deficit theory is more focused on stimulus-valence has not been examined. representations than it is on effective encoding or retrieval of the In considering the encoding-retrieval hypothesis, it seems a stimulus itself. There is also potential overlap between this theory and tenable hypothesis that anhedonia is associated with a lack of the specific anticipatory pleasure deficit (outlined in section one), improved recall ability for pleasant stimuli compared to neutral though the representational deficit theory examines the state-trait stimuli. Such a deficit could explain the state-trait disjunction from an disjunction within a learning theory framework. information processing standpoint, as individuals who lack an The representational deficit theory is supported by two bodies of encoding/recall bias for positive stimuli might be more apt to offer findings. First, evidence suggests that the link between the experience responses downplaying their hedonic experiences when queried. As of stimuli and encoded representations of these experiences is 444 A.S. Cohen et al. / Clinical Psychology Review 31 (2011) 440–448 abnormally disparate in patients with schizophrenia. Heerey and Gold deficits in rapid, but not long-term learning implicated in the (2007) asked stable outpatients with schizophrenia to rate their aforementioned studies, suggest dysfunctions in prefrontal structures. emotional experiences to standardized pleasant, unpleasant and Of note, dorsolateral pre-frontal cortical structures are thought to play neutral picture stills. They were also asked to make speeded button a critical role in delay discounting abilities (Bjork, Momenan, & presses in the absence of each stimulus to indicate whether they Hommer, 2009) and orbitofrontal structures are implicated in wished to see it again. Consistent with the larger literature on state updating and “on-line” adaptation to changing contingencies as hedonic experience in schizophrenia, these patients reported similar used by “rapid” learning systems (Schoenbaum, Roesch, & Stalnaker, subjective hedonic ratings to the stimuli as controls. In contrast to 2006). That these systems are largely dopaminergic in nature—a controls, who showed significant changes in button pressing central to schizophrenia pathology—and that other behaviors across the pleasant, unpleasant and neutral stimuli, patients neuropsychological functions involving these regions are impaired, showed little behavioral change across these conditions. That is, such as working memory and context processing (Barch, Carter, patients showed a relatively consistent pattern of button pressing MacDonald, Braver, & Cohen, 2003; Park & Holzman, 1992) serves to regardless of the valence of stimuli. Moreover, correlations between further bolster this theory. subjective ratings and button pressing behavior were much higher in the control than the patient group, suggesting that state experience in 6. Social-specific hedonic deficit the presence of the stimuli has a closer tie to that experience in the absence of the stimuli in controls as compared to patients. Studies A final explanation for the state-trait disjunction is that state employing delayed discounting and probabilistic “gambling” decision emotion deficits are largely constrained to specific types of stimuli or making tasks have also supported this notion (e.g., Heerey, Robinson, specific domains. Affective experience can vary across a wide range of McMahon, & Gold, 2007). Individuals with schizophrenia are stimuli, and there is reason to believe that anhedonia in schizophrenia significantly more likely than controls to select smaller immediate is restricted to social domains. In other words, experience of both state rewards over larger payoffs paid at a later date and are more likely to and trait pleasant emotion is disordered in individuals with make much less optimal choices to maximize payoff. Taken together, schizophrenia in response to social stimuli only. Pleasurable experi- these results suggest that individuals with schizophrenia show a ence of non-social stimuli, such as food, movies and cigarettes may deficit in the ability to mentally represent the value of a stimulus, largely be preserved. The social-specific hedonic deficit theory posits whether it is a picture or more tangible reward. Thus, individuals with that the apparent “state-trait” disjunction is due to the fact that prior schizophrenia might be expected to report lower trait pleasurable studies of state pleasant experiencehavelargelyinvestigated experience in the absence of affective stimuli, despite intact state emotional experience in non-social domains. hedonic experience, because they have difficulty utilizing learning Social anhedonia is an important feature of schizophrenia. mechanisms to pair the hedonic reward of past experience with Compared to healthy controls, individuals with schizophrenia abstract representations of those experiences. consistently show elevated levels of social anhedonia using question- The second line of research used to support the representational naire-based assessments (Berenbaum & Oltmanns, 1992; Chapman et deficit theory involves investigating learning in al., 1976) and in patients social anhedonia is associated with poorer schizophrenia. Gold et al. (2008) have proposed that individuals social functioning (Blanchard et al., 1998). Research suggests that with schizophrenia show a differential deficit in “rapid learning social anhedonia reflects a trait-like characteristic of the disorder. For systems,” which involve unexpected changes in reward contingen- example, when assessed over a period of one year, Blanchard, Horan, cies, as compared to relatively intact “long-term knowledge” and Brown (2001) found that in patients social anhedonia remained structures, which involve detection of irregularities over long-term stable even when symptoms remitted. This was not true of individuals stimuli presentations. Data from studies employing measures such as with depression in which anhedonia tended to occur during mood the Wisconsin Card Sorting Test (Prentice, Gold, & Buchanan, 2008), episodes (Blanchard et al., 2001). Furthermore, in patients with the probabilistic reversal learning paradigm (Waltz & Gold, 2007) and schizophrenia, social anhedonia has been positively correlated with the reward sensitivity paradigm (Heerey, Bell-Warren, & Gold, 2008) premorbid functioning rather than clinical status at the time of have demonstrated that patients consistently show abnormally poor testing, while in patients with and depression the performance under conditions of changing reinforcement outcomes. opposite is true (Katsanis, Iacono, Beiser, & Lacey, 1992). There is also These changing contingencies tap rapid learning processes and reason to believe that social anhedonia should be conceptualized and require the ability to develop an abstract, but implicit, representation measured apart from nonsocial or physical anhedonia. In patients of the stimulus valence. In contrast, when reinforcement contingen- with schizophrenia, social anhedonia appears to be distinct from cies are relatively stable over time, promoting the use of long-term physical anhedonia in that social anhedonia is more strongly related knowledge systems, patients with schizophrenia show response to trait negative affect (Blanchard et al., 1998). Blanchard, Bellack, and accuracies similar to controls (Morris, Heerey, Gold, & Holroyd, Mueser (1994) also found that while questionnaire-measured 2008). That is, individuals with schizophrenia can employ feedback to physical anhedonia was related to attenuated pleasure experience effectively learn implicit stimulus-response pairings, but have with non-social stimuli (response to mood-inducing videos), social difficulty updating values attached to these stimuli. Thus, as it is anhedonia was not. Therefore, the abilities to experience social and argued by Gold et al. (2008), dysfunctions in the ability to fully physical pleasure are not redundant with each other. represent the affective value of stimuli, whether it be reinforcing or Social anhedonia appears to also be an important construct for punishing, leads to a differential deficit in decision making and rapid understanding schizophrenia-spectrum liability more generally. From learning. This deficit in mentally representing value in the absence of a theoretical perspective, social anhedonia has been postulated to be the stimulus leads patients to underestimate their predicted an important (but not sufficient) condition for schizophrenia experience. pathology reflecting the product of a cascade of genetic and social The representational deficit theory is consistent with conceptua- learning influences (Meehl, 1990). This theory has contributed to the lizations of the neurobiology of anhedonia and negative symptoms notion that social anhedonia is a marker of illness vulnerability, and more generally. For decades, models of schizophrenia pathology have can help identify “”–a condition present in a putative drawn a link between the and negative symptoms, categorically-distinct subgroup of the population with an estimated including Andreasen's negative syndrome (Andreasen & Olsen, 1982), 10 percent prevalence rate. The specificity of schizophrenia-spectrum Crow's type II schizophrenia (Crow, 1985) and the deficit syndrome anhedonia to social domains as opposed to physical domains was (Kirkpatrick, Buchanan, Ross, & Carpenter, 2001). The differential theorized by Paul Meehl (1990), who noted that “schizoid anhedonia A.S. Cohen et al. / Clinical Psychology Review 31 (2011) 440–448 445 is mainly interpersonal” (p. 833) and that even individuals with and other-report of enjoyment in novel/ambiguous (i.e., going to a schizophrenia experience physical pleasure from sources such as party alone) and highly role-defined (i.e., visiting relatives) activities watching television and smoking cigarettes (Meehl, 1990). In support in both high and low schizotypy individuals. On both measures, the of this conjecture, results from a ten year longitudinal study high schizotypy individuals enjoyed the more ambiguous situations, demonstrate the superiority of a scale assessing social anhedonia but not the highly role-defined activities, significantly less than the over one assessing physical anhedonia for predicting of schizophre- low schizotypy individuals. This is consistent with the argument that nia-spectrum disorders (Kwapil, 1998). Social anhedonia is also that schizophrenia spectrum anhedonia may be specifically social due associated with a number of schizophrenia-like maladies including to the inherent ambiguity of social situations, especially in light of the impaired neurocognition (Cohen, Leung, Saperstein, & Blanchard, above-cited research suggesting that for individuals on the schizo- 2006; Gooding & Braun, 2004; Gooding & Tallent, 2003), physiological phrenia spectrum interpretation of social stimuli may be much more (Gooding, Shea, & Matts, 2005; Simons & Katkin, 1985) and genetic effortful and less intuitive. This may be the factor that leads to less (Docherty & Sponheim, 2008) anomalies. In this regard, social pleasure in social situations (i.e. aversive drift; Meehl, 1990). Support anhedonia appears to reflect a trait-like vulnerability to schizophrenia for this idea is further garnered by research suggesting that spectrum disorders. individuals with schizotypy have difficulty identifying emotions in The social cognition literature is also rapidly growing and offering neutral and low intensity facial expression (the more ambiguous insight into potential structures and pathways involved in processing stimuli) rather than more obvious, higher intensity emotions (Brown social information. In the scientific literature concerning autism, a & Cohen, 2010). disorder that behaviorally resembles the negative/deficit subtype of Another study (Kwapil et al., 2009) examined social experience schizophrenia, some have made the case that limbic structures, using an Experience Sampling Methodology. College students who notably the amygdala are important in understanding social deficits. scored higher on the Revised Social Anhedonia Scale were more likely This is relevant in that both patients with schizophrenia and at-risk to be alone, to prefer being alone, and to report more positive individuals show decreased amygdala volume compared to controls emotions and less negative emotions when alone than with other (Bogerts, Lieberman, Ashtari, & Bilder, 1993; Keshavan et al., 2002; people. Finally, in a study of explicit and implicit measures of social Velakoulis et al., 2006; Wright et al., 2000). Also, a few studies of affectivity in schizotypy, individuals with schizotypy reported patients with schizophrenia have shown decreased activation of the decreased experience of pleasure and increased experience of amygdala in response to social emotional stimuli in the form of facial negative emotions compared to controls when asked explicitly and expressions (Kosaka et al., 2002) with corresponding overactivation during a laboratory-based mood-induction procedure. Interestingly, a of prefrontal regions (Fakra, Salgado-Pineda, Delaveau, Hariri, & Blin, different pattern of results was observed with implicit measures of 2008). This is consistent with a more effortful approach to emotion (Cohen et al., Under Review), using lexical analysis of natural interpretation of social stimuli in comparison with a more intuitive speech as subjects discussed their social relationships and an Implicit processing demonstrated by control participants, suggesting that Association Test specially designed to examine implicit associations these neurobiological abnormalities maybe especially manifest when between valence categories (i.e., “good,”“neutral”)andsocial patients have to interpret social stimuli. categories (i.e., “brother,”“friend”). Individuals with schizotypy and To our knowledge, only a handful of studies has directly examined controls did not differ on any of these measures. These data provide whether social hedonic state experience is compromised in indivi- further evidence that “state” social anhedonia is present in individuals duals with schizophrenia-spectrum pathology. The only study we are with schizotypy, but that it occurs at a higher-order, more evaluative aware of to examine social hedonic experience in schizophrenia level rather than at a basic, automatic level. patients using “in the moment” assessment under controlled In summary, it seems possible that particular aspects of social laboratory experiences (Aghevli, Blanchard, & Horan, 2003) did not stimuli make them difficult to process for individuals with schizo- find evidence for decreased experience of emotion in social situations phrenia spectrum pathology. This may reflect a core deficit in the in individuals with schizophrenia, only less emotional expressivity ability to enjoy social situations in the moment. Alternatively, these (i.e., facial expressions, hand gestures). Limitations of this study social-specific affective dysfunctions may reflect the inherent ambi- include a rather modest sample (n=33) composed exclusively of guity and unpredictability of social situations, and also social cognitive male patients with schizophrenia. Moreover, the study used a social deficits and/or biases. In this regard, it is not clear whether it is “social” role play task to elicit emotions. Given potential cognitive limitations stimuli per se that are difficult to process, or whether it is the inherent of patients with schizophrenia, including abstract representation, it is complexity or ambiguity of social stimuli. Though our knowledge of possible the role play was processed differently than in a genuine these processes remains incomplete, especially concerning etiological social interaction. For example, patients may have engaged in more factors and neural mechanisms involved in social anhedonia, effortful cognitive processing of the task (i.e., interpreting and advances in the affective experience and social cognitive literatures remembering instructions, recalling past instances of similar social lend support to the idea that state social anhedonia is an important situations in real life). Furthermore, there is evidence that some aspect of schizophrenia spectrum pathology. Also unclear is whether individuals with schizophrenia (specifically paranoid) interpret non- individuals with schizophrenia show the same pattern of social genuine social stimuli differently than genuine stimuli (Davis & affective experience as those with schizotypy. The single study of Gibson, 2000). It is possible that some patients had more difficulty schizophrenia patients discussed above (Aghevli et al., 2003), than controls interpreting the role play as they would a real social although limited in some respects, suggests not. Thus, there is situation. Additional studies are needed to examine whether these evidence of state social anhedonia in individuals with schizotypy findings replicate in larger samples including female patients using but not for patients with schizophrenia. It is possible that individuals other social stimuli. Further research should also examine emotional with schizotypy may have better insight into their social oddities or experience in social situations across different subtypes of schizo- impaired social cognitive abilities which may limit these individuals' phrenia, especially those with negative symptoms. ability to experience pleasure due to interfering negative emotions. A handful of other “laboratory”-based studies has been conducted More research is needed specifically on the "in the moment" affective on individuals with schizotypy. Quirk, Subramanian, and Hoerger experience of social stimuli in individuals with schizotypy and (2007) found that individuals at risk for schizophrenia report less controls. Measures of self-confidence or perceived social skill may enjoyment from ambiguous social situations than healthy controls, help clarify whether it is those situations in which schizophrenia perhaps suggesting that individuals lacking the resources to navigate spectrum individuals feel less competent or at ease that elicit less ambiguous situations enjoy them less. These authors examined self- pleasure. It may also be the case that a lack of or deficient affiliative 446 A.S. Cohen et al. / Clinical Psychology Review 31 (2011) 440–448 tendency in combination with limited neurocognitive resources leads methods from cognitive and social psychology, basic emotion, to a decreased social responsiveness and “aversive drift” in schizo- neuroscience/neurobiology and other fields has paved the way for phrenia spectrum individuals (see Meehl, 1962 for elaboration). More new insights. Further advances in understanding the affective deficits research in all domains concerning the social life of schizophrenia in schizophrenia will only be possible through similar multidisciplin- spectrum individuals (social cognition, emotional processing, social ary research. behavior, underlying neural pathways) with corresponding integra- fi tion of these ndings is needed. References

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