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Stability of cognition across wakefulness and dreams in psychotic major depression
Psychiatry Research 216 (2014) 31–36
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Stability of cognition across wakefulness and dreams in psychotic major depression Simone Cavallotti a,b, Anna Castelnovo a,b, Rebecca Ranieri a,b, Armando D'Agostino a,b,n a b
Department of Mental Health, San Paolo Hospital, Milan, Italy Department of Health Sciences, Università degli Studi di Milano, Italy
art ic l e i nf o
a b s t r a c t
Article history: Received 25 January 2013 Received in revised form 30 November 2013 Accepted 21 January 2014 Available online 30 January 2014
Cognitive bizarreness has been shown to be equally elevated in the dream and waking mentation of acutely symptomatic inpatients diagnosed with affective and non-affective psychoses. Although some studies have reported on dream content in non-psychotic depression, no study has previously measured this formal aspect of cognition in patients hospitalized for Psychotic Major Depression (PMD). Sixty-five dreams and 154 waking fantasy reports were collected from 11 PMD inpatients and 11 age- and sexmatched healthy controls. All narrative reports were scored by judges blind to diagnosis in terms of formal aspects of cognition (Bizarreness). Dream content was also scored (Hall/Van de Castle scoring system). Unlike controls, PMD patients had similar levels of cognitive bizarreness in their dream and waking mentation. Dreams of PMD patients also differed from those of controls in terms of content variables. In particular, Happiness, Apprehension and Dynamism were found to differ between the two groups. Whereas dream content reflects a sharp discontinuity with the depressive state, cognitive bizarreness adequately measures the stability of cognition across dreams and wakefulness in PMD inpatients. & 2014 Elsevier Ireland Ltd. All rights reserved.
Keywords: Psychosis Dreaming Cognitive bizarreness Dream content REM sleep Mood disorders
1. Introduction 1.1. Cognitive bizarreness in dreams and psychosis Most of the founders of contemporary psychiatry observed significant similarities between dreams and the subjective experience of psychosis (Kraepelin, 1906; Bleuler 1966). In both conditions, subjects fail to recognize the internal origin of perceived stimuli that are interpreted as coming from the external environment; heightened and often incongruous emotions are coupled with a decrease in ego functions which ultimately leads to instinctual behaviours and severe impairment in reality testing (Hobson, 2009). The progression from salience attributed to irrelevant stimuli to a new, highly relevant meaning that occurs in psychosis can also be observed in dreams, where a single hallucinatory image can convey “an immediate emotionally compelling meaning that is not related to the image in any obvious way” (Feinberg, 2011). Of course, several differences can also be observed between the two states. First of all, dreaming occurs in the context of sleep when the subject is detached from the environment. In the course of so-called functional (i.e. nonn Correspondence to: Dipartimento di Salute Mentale, A.O. San Paolo, via Antonio di Rudinì 8, 20142 Milan, Italy. Tel.: þ39 02 81844516; fax: þ39 02 81844026. E-mail address: [email protected] (A. D'Agostino).
0165-1781/$ - see front matter & 2014 Elsevier Ireland Ltd. All rights reserved. http://dx.doi.org/10.1016/j.psychres.2014.01.033
organic) psychoses, symptoms occur in clear consciousness and patients tend to maintain a valid contact with the external world. Second, the hallucinatory product of the dreaming brain is primarily visual whereas psychosis in psychiatric patients is usually characterized by auditory hallucinations. Current research in the phenomenology and neurobiology of dreams has proved a fertile ground for a reanalysis of this relationship, and several hypotheses binding these phenomena have been proposed (Hobson, 2004; Gottesmann, 2006; Feinberg, 2011). However, the scientific validity and meaning of the dream/psychosis relationship is yet to be fully understood. Cognitive bizarreness, a measurable aspect of the formal organization of dream mentation, has been shown to be equally elevated in the dreams and waking fantasies of acutely symptomatic inpatients diagnosed with either Schizophrenia or the manic phase of Bipolar Disorder (Scarone et al., 2008; Limosani et al., 2011). Our group hypothesized these findings could provide evidence of shared cognitive patterns in dreams and psychosis independent of the disorder within which symptoms emerge (D’Agostino et al., 2012). To the best of our knowledge, no similar data have been collected in patients with psychotic symptoms in the context of a depressive episode. Unipolar Major Depression with Psychotic Features, or Psychotic Major Depression (PMD), can be diagnosed in up to 19% of all subjects with an episode of unipolar depression (Ohayon and Schatzberg, 2002). Delusions and/or
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hallucinations in these patients are associated with less responsiveness to medication, worse prognosis and higher rates of neurobiological and neuropsychological abnormalities (Hill et al., 2004). The widespread clinical assumption that psychotic symptoms in PMD depend on the severity of a depressive episode has not been confirmed by recent research, which seems to bind this clinical phenomenon to a biological and/or psychosocial individual susceptibility (Forty et al., 2009). 1.2. Known peculiarities of dream content in depressed patients Although several previous studies assessed the dreams of depressed patients, none have reported on those of PMD patients. Dreams of inpatients with severe unipolar depression have been found to be less bizarre but more mundane and flat in terms of affective content when compared to those of a control population (Beauchemin and Hays, 1996). Dream reports have been found to be shorter during depressive episodes (Barrett and Loeffler, 1992; Fonzi et al., 2006) and content variables such as emotional tone and anxiety levels have been correlated to clinical progression and outcome in several studies. In general, dream emotion appears to reflect predominant waking emotion, so that negatively toned and anxious dreams are more common in patients who report high levels of anxiety and depressed affect than in the general population (Cartwright and Lloyd, 1994; Beauchemin and Hays, 1996; Cartwright et al., 1998; Bilici et al., 2002). Improvement in clinical symptoms was also associated to a progressive normalization of the emotional tone observed in dream reports (Fonzi et al., 2006; Schredl et al., 2009). 1.3. Study objectives Main objectives of this study were (1) to evaluate cognitive bizarreness in the dreams and waking fantasies of PMD inpatients compared to a normal control population and (2) to identify similarities and differences in dream content in the same sample. We hypothesized that the waking cognition of these subjects would yield similarly elevated levels of cognitive bizarreness to those found in dreams, whereas no specific prediction was made in terms of dream content variables.
2. Methods 2.1. Patients Patients were recruited from the psychiatric ward of the San Paolo Hospital Department of Mental Health. Participants were male or female inpatients of at least 18 years of age, who met the DSM-IV-TR criteria for an Axis I diagnosis of Major Depressive Episode with Psychotic Symptoms (APA, 2000). All patients' diagnoses were assessed by means of the criteria of the Structured Clinical Interview for DSM-IV Axis I Disorders (First et al., 1997). Eleven patients (three M, eight F; mean age 53.647 12) completed the experimental protocol, so a group of 11 subjects matched in terms of sex and age (three M, eight F; mean age 53.36 7 11.27) were chosen from the general population as control sample. Exclusion criteria for both groups were alcohol and psychoactive substance abuse and a present or past history of any serious medical or neurological condition, including perinatal injury, cranial trauma, mental retardation and parasomnias. Patients who met diagnostic criteria for any other Axis I or Axis II disorder were excluded, so none of the patients enroled had ever received a diagnosis of Bipolar Disorder. Control subjects were unpaid volunteers recruited by word of mouth among the general population. They were only enroled if history of clinically relevant depression or psychosis could be ruled out with certainty after a clinical interview carried out by a certified psychiatrist. 2.2. Clinical assessment Clinical assessment was performed by one expert psychiatrist using the 21item Hamilton Depression Rating Scale—HAM-D-21 (Hamilton, 1967) and 18-item Brief Psychiatric Rating Scale—BPRS (Overall & Gorham, 1962). The scales were
administered before significant remission of symptoms, during the week in which patients were asked to keep a dream diary, which usually began upon admission. The mean score obtained in HAM-D (277 5.74) suggests severe depression in our sample. All patients scored between 5 and 7 on the “unusual thought content” item of the BPRS and presented with guilt, persecution, ruin and somatic delusions. 2.3. Pharmacotherapy None of the patients included in the study were drug-naïve; administration of treatment began at the moment of admission to our unit as prescribed by the assigned physician. Various combinations of antidepressants (all patients were treated with SSRIs), antipsychotics and benzodiazepines were administered to all patients during the week in which the material for the study was collected. 2.4. Study design All participants were asked to sign an informed consent to take part in the study. During the first week of hospitalization, patients were instructed to keep a dream diary where they could report each morning the dream they had had the night before. As instruction, participants were asked to report the whole development of the dream plot whenever possible. The material was always collected during the first week of hospitalization, before significant remission of the psychotic symptoms, whereas the control population completed dream diaries in their home setting. Subjects who successfully reported at least one dream were then administered a projective test used to elicit fantasy stories. The Thematic Apperception Test (TAT) consists of a broad set of figures, differentiated into groups of 20 according to sex and age (Murray, 1943). Seven figures chosen progressively from the full set were used in this study according to a previously published scheme (Scarone et al., 2008; Limosani et al., 2011; D’Agostino et al., 2012). Given that several authors have questioned the reliability and validity of the test's psychometric properties (Cramer, 1999), the TAT was only used in this study design to elicit waking fantasies from a standardized set of stimuli. All participants were asked to create a fantasy story that clearly contained a beginning, a plot development and an end based on the visualized figure after having eliminated the stimulus; the narratives created in response to the fixed stimulus were tape-recorded and then transcribed. 2.5. Formal analysis of narratives A total of 65 dream reports (25 belonging to depressed patients and 40 belonging to the control group) and 168 waking fantasy reports (84 for each group) were collected for analysis. The material was equally divided and randomly assigned to two judges who had no acquaintance with the study participants and were blind to the diagnosis and to the origin of the narrative transcripts. The Dream Bizarreness scale (Hobson et al., 1987) was used to score the material as described elsewhere (Scarone et al., 2008, Limosani et al., 2011). The following indices were calculated for each dream and TAT response: bizarreness intensity (BI), calculated as the number of bizarre events in the domains of plot, cognition, and affect, and bizarreness density (BD), calculated by dividing BI by the report word count. The following indices were then calculated for each subject, yielding normally distributed data: Bizarreness Density Index for dreams (BDI), calculated as the mean of the dream BD indices, and Bizarreness Density Index for TAT tables (BDI), calculated as the mean of the TAT table BD indices. 2.6. Dream content analysis The Hall/Van de Castle scoring system was used to analyse dream contents (Hall, Van de Castle, 1966). This scale is considered to be the most comprehensive and used empirical system for dream content analysis, with several nominal categories reflecting characters, aggressiveness, social interactions, emotions, etc. within the dream report (Domhoff, 1996). According to a previously published method, each content category was represented by a number reflecting the frequency of a given content within a dream report. An average index was developed for each participant based on the number of reported dreams. Scoring was undergone by one group-blind judge who was adequately trained in the use of the scale (Scarone et al., 2008; Limosani et al., 2011). 2.7. Statistical analyses All data analyses were performed with SPSS version 19.0 (IBM, 2010). Two-way Analysis of Variance (ANOVA) for repeated measures was applied to assess the effect of diagnosis and experimental study conditions (TAT stories and dream reports) on cognitive bizarreness. Pearson's correlation coefficient was used to measure the strength of the linear relationship between HAM-D-21 total score and BDI scores in the patient sample. Analysis of Variance (ANOVA) was applied to assess the effect of diagnosis on the content scored in dream reports using the Hall/
S. Cavallotti et al. / Psychiatry Research 216 (2014) 31–36 Van de Castle system. Content categories were treated as dependent variables with diagnosis as the fixed factor.
3. Results 3.1. Bizarreness in dream and waking fantasy reports Fig. 1 shows the means of dream and TAT BDIs in depressed and normal subjects. The interaction between the experimental conditions and diagnosis was highly significant (F1,20 ¼18.35, po0.01). Depressed patients had similar levels of cognitive bizarreness in their dream (BDI: M¼ 0.024, S.D.¼0.02) and waking (BDI: M¼0.025, S.D.¼0.01) mentation, whereas control subjects had a higher level in dreams (BDI: M¼0.038, S.D.¼0.01) and almost no bizarreness in wakefulness (BDI: M¼0.009, S.D.¼ 0.01). Independent-samples t-tests were conducted to compare BDI values in the two samples
Fig. 1. Mean BDI values in the wakefulness and dreams of patients diagnosed with PMD and healthy control subjects.
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across experimental conditions. Dream bizarreness was found to be significantly lower in the PMD group compared to the control group (t(20)¼2.83, po0.05). Within the control group, dream bizarreness was found to be significantly higher than waking bizarreness (t(20)¼ 7.99, po0.01). Finally, no significant difference could be found between dream and waking bizarreness bizarreness within the PMD group (t(20)¼ 0.18, p¼n.s.). Within the patient group, no correlation could be found between dream BDI and HAM-D-21 total score (r ¼ 0.41, p ¼n.s.) nor between BDI and HAM-D-21 total score (r ¼0.17, p ¼n.s.).
3.2. Length of reports and dream content Dream report length was found to be shorter in depressed individuals (M¼96.7, S.D.¼80) than in the healthy control population (M¼147.7, S.D.¼79). An independent-samples t-test conducted to compare dream report lengths in the two samples yielded no significant difference: t(20)¼ 1.5, p¼ 0.993. Therefore, no specific correction was necessary for content analysis. TAT reports were generally shorter than dream reports in both groups (Depressed subjects: M¼39.09, S.D.¼11.25; Control subjects: M¼56.3, S.D.¼32.2). An independent-samples t-test was conducted to compare TAT report lengths in the two samples. The observed difference was found to be statistically significant: t(20)¼ 1.67, po0.05. Fig. 2 shows the means of the indexes which refer to each content category scored with the Hall/Van de Castle system in depressed patients and normal controls. ANOVA yielded a significant Between-groups effect for three specific variables: Happiness (HA) (F1,21 ¼ 4.43, po0.05), Apprehension (AP) (F1,21 ¼7.43, po0.05) and Dynamism (DYN) (F1,21 ¼10.34, po0.05). Whereas the first was relatively frequent in the dreams of depressed patients (HA: M¼0.21, S.D.¼ 0.33), it was never scored in the control group (HA: M¼0). On the contrary, the latter two recurred with lower frequency in the patient sample (AP: M¼ 0.12, S.D.¼0.21; DYN: M¼0.42, S.D.¼0.71) compared to the control group (AP: M¼ 0.65, S.D.¼0.61; DYN: M¼1.47, S.D.¼0.82).
Fig. 2. Dream content in patients diagnosed with PMD and healthy control subjects according to the Hall/van de Castle scoring system. between the two groups.
n
Statistically significant differences
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4. Discussion 4.1. Stability of cognition across wakefulness and dreams In terms of formal aspects of cognition, bizarreness was found to be surprisingly stable across waking fantasies and dreams in PMD inpatients. This finding suggests that acutely psychotic subjects have similar levels of cognitive bizarreness in dream reports and verbal reports elicited by the TAT. Hence, this cognitive pattern that has been supposed to reflect underlying neurofunctional modifications (Mamelak and Hobson, 1986) could also be considered a distinctive formal property of the waking cognitive organization of psychosis. Our preliminary results on PMD patients dovetail nicely with previous finding in schizophrenic (Scarone et al., 2008) and manic (Limosani et al., 2011) subjects with acute psychotic symptoms. However, as clearly shown in Fig. 1, dream and waking levels of bizarreness in PMD patients are intermediate between the high level of dream bizarreness and the very low level found in the waking fantasies of the control population. This confirms previous findings in non-psychotic depressed patients, where dream bizarreness was lower compared to that of healthy subjects (Beauchemin and Hays, 1996).
(Hobson, 2009; Stephan, Friston and Frith, 2009; Wiffen and David, 2009). This deficit sustains the subject's firm belief in the truthfulness of his experience, be it a dream in which his house resembles his childhood school or the delusional idea that his body has transformed into a mass of rotting organs. The formal construction of dreams and psychotic processes measured as bizarreness could reflect a common underlying neurobiological mechanism by which the brain/mind loses its ability to engage a logical relationship with the external environment in the processing of incoming information (Corlett et al., 2010). Several neurophysiological, neurochemical and cerebrofunctional patterns of activity suggest similarities between dreaming and psychosis. Overlapping findings in these two conditions have been discussed elsewhere (D’Agostino et al., 2012). Hyperactivation of the dopaminergic reward system has recently been proposed to play a central role in the generation of dreams (Perogamvros and Schwartz, 2012). The same type of brain activity is broadly accepted as a final common pathway of several disturbances that lead to psychosis (Howes and Kapur, 2009). Indeed, aberrant attribution of salience to one's own experience coupled with impaired elaboration of prediction errors dependent on a hyperactive dopaminergic system can explain most phenomenological features of both dreams and psychosis.
4.2. Relationship between cognitive bizarreness and psychosis Cognitive bizarreness reflects discontinuous, incongruous and vague transitions within a report comprising thoughts, emotions and narrative plot (Hobson et al., 1987; Stickgold et al., 1994). Although some data suggest that waking imagery can contain bizarre elements (Klinger and Cox, 1987; Kane et al., 2007; Klinger, 2008), or even that waking imagery can be more bizarre than dreaming (Reinsel et al., 1992; Wollman and Antrobus, 1986), most studies confirm that bizarre elements are more prevalent in dreams than in waking imagery (Williams et al., 1992; Cicogna et al., 2007; Scarone et al., 2008; Limosani et al., 2011; Kahan and LaBerge, 2011). Moreover, although “thin boundary” personality has been related to more bizarre dreams and daydreams than “thick boundary”, as a whole dreams were found to be more bizarre than daydreams across both personality types (Kunzendorf et al., 1997), further strengthening the common assumption that cognitive bizarreness is a distinguishing feature of dreams. It has been observed that the few studies in which waking mentation appeared to be more bizarre adopted a sensory restriction protocol that could have influenced findings (Hobson et al., 2000). Indeed, subjects were asked to report imaginative experiences in a condition of darkness and sound restriction that is known to trigger psychotomimetic symptoms in healthy volunteers within 15 min (Mason and Brady, 2009). The recurrence of bizarreness in the waking mentation of acute psychotic patients belonging to different diagnostic domains warrants a closer discussion of its meaning. This peculiar type of cognition was originally attributed to the loss of noradrenergic modulation of the cortex (Hartmann, 1973) or the spontaneous activity of the brain as a closed system in absence of environmental inputs and voluntary self-regulation mechanisms (Rechtschaffen, 1978; Antrobus, 1991). More recently, it was correlated to the ponto-geniculo-occipital waves that have been recorded when cholinergic hyperactivity triggers REM sleep in the absence of aminergic inhibition (Quattrochi et al. 1998). In terms of functional activation in this stage of sleep, where bizarreness has been found to be highest, recent findings suggest a relationship between dream bizarreness and the decrease in temporal coupling between executive and perceptual regions of the cortex (Corsi-Cabrera et al., 2003). In psychosis and dreams alike, the subject's inability to discern the origin of emotion and perception-related internal sources appears to reflect a deficit of self-monitoring mechanisms mediated by the frontal lobes
4.3. Emotional tone in PMD dreams In terms of content, relevant peculiarities could be identified within the emotional tone of dreams. Surprisingly, dreams of PMD patients reflected more Happiness and less Apprehension compared to those of the control population. Despite some controversy amongst researchers, it is generally accepted that negative emotions such as sadness and apprehension outweigh positive ones in the dreams of healthy subjects (Schredl and Doll, 1998). Previous studies in non-psychotic depressed patients all report an intensification of such imbalance that has been interpreted as proof of continuity in emotional tone within subjects in wakefulness and dreams (Schredl et al., 2009). Untreated patients have been found to report dreams with more depressive contents when awoken from REM stages in the latter part of the night (Agargun and Cartwright, 2003) and the spontaneous dream recall upon awakening used in our protocol is generally thought to reflect the most recent oneiric episode of the night. The inversion of this balance in the dreams of patients with PMD could be interpreted as evidence of a pronounced affective dysregulation across the sleep/wake cycle in this population. Indeed, PMD has been found to be characterized by more severe REM sleep abnormalities when compared to non-psychotic depression (Thase et al., 1986). Although REM sleep is thought to promote consolidation of emotionally salient memories (Nishida et al. 2009), no speculations can be made on the basis of our findings given that sleep stage was not controlled. One other possible explanation of our finding is that positive dream emotions depend on the patients' antidepressant medication (see following section for a full discussion on the effect of psychotropic drugs on sleep and dreams). Indeed, one previous study found dream emotion to improve during the course of treatment with tricyclic antidepressant trimipramine (Schredl et al., 2009). However, previous findings suggest that dream emotion improvement parallels clinical improvement in nonpsychotic depressed patients, whereas our population presented severe depression with psychotic symptoms at the time of dream collection. More intuitively, the reduced Dynamism observed in the dreams of PMD patients can be interpreted as continuous with the typical psychomotor retardation of depressive syndromes.
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4.4. Methodological issues
References
Several limitations should be considered in discussing these preliminary results. First of all, enroled patients were on treatment with psychoactive drugs which might have influenced both the form and content both of dreams and waking fantasies. Dream recall frequency is known to decrease in depressed patients treated with all classes of antidepressant drugs, independent of drug-specific effects on REM sleep (Schredl et al., 2009). Antidepressant drugs could also influence the emotional tone of dreams. Available data are often contradictory and some authors report increased positive dream content associated with improvement in clinical symptoms (Schredl et al., 2009), whereas others describe no changes in dream content despite clinical improvement (Armitage et al., 1995). According to a recent review, the most consistent findings are that tricyclic antidepressants induce more positive dream emotions and that Selective Serotonin Reuptake Inhibitors (SSRIs) have a dream intensifying effect and may elicit more dream material (Tribl et al., 2012). In this study, all patients were treated with SSRIs that are known to suppress REM sleep (Wilson and Argyropoulos, 2005). Most patients were also treated with variable doses of benzodiazepinic agents that are also known to suppress both Slow Wave Sleep and REM sleep (Achermann and Borbély, 1987; Borbély et al., 1985; Gaillard et al., 1973) This may at least in part account for the intermediate levels of bizarreness found in their dreams. Regarding antipsychotic medications, it should be noted that the influence of these molecules on REM–NREM sleep architecture are still inconclusive (Nofzinger and Keshavan, 2002). A second relevant issue in our design is the lack of a control group of patients diagnosed with Major Depression without Psychotic features. Indeed, the present study design cannot exclude that observed levels of cognitive bizarreness depend on the depressive state rather than psychotic symptoms. Although bizarreness has been found to diminish in the dreams of depressed patients (Beauchemin and Hays, 1996), no previous studies analysed its expression during wakefulness in this population. Future studies with a three-group design will help to at least partially control for the effect of both medication and specific mood disorder on the results. A third issue that limits our findings regards the small sample of patients enroled in the study and the low number of dreams analysed.
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4.5. Conclusive remarks In conclusion, the present preliminary study appears to suggest that cognitive bizarreness can adequately measure the stability of cognition across dreams and wakefulness in acutely psychotic inpatients. With specific reference to PMD, dream content was found here to be surprisingly more positive in terms of emotional tone when compared to that of the general population and of previous reports in nonpsychotic depressed patients. This intriguing finding warrants further investigation and could reflect a discontinuity with waking emotion in these subjects.
Role of funding source None.
Acknowledgements The authors would like to thank Drs. Ivan Limosani and Maria Laura Manzone for their helpful discussions and their contribution to recruitment of control subjects.
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Stability of cognition across wakefulness and dreams in psychotic major depression Simone Cavallotti a,b, Anna Castelnovo a,b, Rebecca Ranieri a,b, Armando D'Agostino a,b,n a b
Department of Mental Health, San Paolo Hospital, Milan, Italy Department of Health Sciences, Università degli Studi di Milano, Italy
art ic l e i nf o
a b s t r a c t
Article history: Received 25 January 2013 Received in revised form 30 November 2013 Accepted 21 January 2014 Available online 30 January 2014
Cognitive bizarreness has been shown to be equally elevated in the dream and waking mentation of acutely symptomatic inpatients diagnosed with affective and non-affective psychoses. Although some studies have reported on dream content in non-psychotic depression, no study has previously measured this formal aspect of cognition in patients hospitalized for Psychotic Major Depression (PMD). Sixty-five dreams and 154 waking fantasy reports were collected from 11 PMD inpatients and 11 age- and sexmatched healthy controls. All narrative reports were scored by judges blind to diagnosis in terms of formal aspects of cognition (Bizarreness). Dream content was also scored (Hall/Van de Castle scoring system). Unlike controls, PMD patients had similar levels of cognitive bizarreness in their dream and waking mentation. Dreams of PMD patients also differed from those of controls in terms of content variables. In particular, Happiness, Apprehension and Dynamism were found to differ between the two groups. Whereas dream content reflects a sharp discontinuity with the depressive state, cognitive bizarreness adequately measures the stability of cognition across dreams and wakefulness in PMD inpatients. & 2014 Elsevier Ireland Ltd. All rights reserved.
Keywords: Psychosis Dreaming Cognitive bizarreness Dream content REM sleep Mood disorders
1. Introduction 1.1. Cognitive bizarreness in dreams and psychosis Most of the founders of contemporary psychiatry observed significant similarities between dreams and the subjective experience of psychosis (Kraepelin, 1906; Bleuler 1966). In both conditions, subjects fail to recognize the internal origin of perceived stimuli that are interpreted as coming from the external environment; heightened and often incongruous emotions are coupled with a decrease in ego functions which ultimately leads to instinctual behaviours and severe impairment in reality testing (Hobson, 2009). The progression from salience attributed to irrelevant stimuli to a new, highly relevant meaning that occurs in psychosis can also be observed in dreams, where a single hallucinatory image can convey “an immediate emotionally compelling meaning that is not related to the image in any obvious way” (Feinberg, 2011). Of course, several differences can also be observed between the two states. First of all, dreaming occurs in the context of sleep when the subject is detached from the environment. In the course of so-called functional (i.e. nonn Correspondence to: Dipartimento di Salute Mentale, A.O. San Paolo, via Antonio di Rudinì 8, 20142 Milan, Italy. Tel.: þ39 02 81844516; fax: þ39 02 81844026. E-mail address: [email protected] (A. D'Agostino).
0165-1781/$ - see front matter & 2014 Elsevier Ireland Ltd. All rights reserved. http://dx.doi.org/10.1016/j.psychres.2014.01.033
organic) psychoses, symptoms occur in clear consciousness and patients tend to maintain a valid contact with the external world. Second, the hallucinatory product of the dreaming brain is primarily visual whereas psychosis in psychiatric patients is usually characterized by auditory hallucinations. Current research in the phenomenology and neurobiology of dreams has proved a fertile ground for a reanalysis of this relationship, and several hypotheses binding these phenomena have been proposed (Hobson, 2004; Gottesmann, 2006; Feinberg, 2011). However, the scientific validity and meaning of the dream/psychosis relationship is yet to be fully understood. Cognitive bizarreness, a measurable aspect of the formal organization of dream mentation, has been shown to be equally elevated in the dreams and waking fantasies of acutely symptomatic inpatients diagnosed with either Schizophrenia or the manic phase of Bipolar Disorder (Scarone et al., 2008; Limosani et al., 2011). Our group hypothesized these findings could provide evidence of shared cognitive patterns in dreams and psychosis independent of the disorder within which symptoms emerge (D’Agostino et al., 2012). To the best of our knowledge, no similar data have been collected in patients with psychotic symptoms in the context of a depressive episode. Unipolar Major Depression with Psychotic Features, or Psychotic Major Depression (PMD), can be diagnosed in up to 19% of all subjects with an episode of unipolar depression (Ohayon and Schatzberg, 2002). Delusions and/or
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hallucinations in these patients are associated with less responsiveness to medication, worse prognosis and higher rates of neurobiological and neuropsychological abnormalities (Hill et al., 2004). The widespread clinical assumption that psychotic symptoms in PMD depend on the severity of a depressive episode has not been confirmed by recent research, which seems to bind this clinical phenomenon to a biological and/or psychosocial individual susceptibility (Forty et al., 2009). 1.2. Known peculiarities of dream content in depressed patients Although several previous studies assessed the dreams of depressed patients, none have reported on those of PMD patients. Dreams of inpatients with severe unipolar depression have been found to be less bizarre but more mundane and flat in terms of affective content when compared to those of a control population (Beauchemin and Hays, 1996). Dream reports have been found to be shorter during depressive episodes (Barrett and Loeffler, 1992; Fonzi et al., 2006) and content variables such as emotional tone and anxiety levels have been correlated to clinical progression and outcome in several studies. In general, dream emotion appears to reflect predominant waking emotion, so that negatively toned and anxious dreams are more common in patients who report high levels of anxiety and depressed affect than in the general population (Cartwright and Lloyd, 1994; Beauchemin and Hays, 1996; Cartwright et al., 1998; Bilici et al., 2002). Improvement in clinical symptoms was also associated to a progressive normalization of the emotional tone observed in dream reports (Fonzi et al., 2006; Schredl et al., 2009). 1.3. Study objectives Main objectives of this study were (1) to evaluate cognitive bizarreness in the dreams and waking fantasies of PMD inpatients compared to a normal control population and (2) to identify similarities and differences in dream content in the same sample. We hypothesized that the waking cognition of these subjects would yield similarly elevated levels of cognitive bizarreness to those found in dreams, whereas no specific prediction was made in terms of dream content variables.
2. Methods 2.1. Patients Patients were recruited from the psychiatric ward of the San Paolo Hospital Department of Mental Health. Participants were male or female inpatients of at least 18 years of age, who met the DSM-IV-TR criteria for an Axis I diagnosis of Major Depressive Episode with Psychotic Symptoms (APA, 2000). All patients' diagnoses were assessed by means of the criteria of the Structured Clinical Interview for DSM-IV Axis I Disorders (First et al., 1997). Eleven patients (three M, eight F; mean age 53.647 12) completed the experimental protocol, so a group of 11 subjects matched in terms of sex and age (three M, eight F; mean age 53.36 7 11.27) were chosen from the general population as control sample. Exclusion criteria for both groups were alcohol and psychoactive substance abuse and a present or past history of any serious medical or neurological condition, including perinatal injury, cranial trauma, mental retardation and parasomnias. Patients who met diagnostic criteria for any other Axis I or Axis II disorder were excluded, so none of the patients enroled had ever received a diagnosis of Bipolar Disorder. Control subjects were unpaid volunteers recruited by word of mouth among the general population. They were only enroled if history of clinically relevant depression or psychosis could be ruled out with certainty after a clinical interview carried out by a certified psychiatrist. 2.2. Clinical assessment Clinical assessment was performed by one expert psychiatrist using the 21item Hamilton Depression Rating Scale—HAM-D-21 (Hamilton, 1967) and 18-item Brief Psychiatric Rating Scale—BPRS (Overall & Gorham, 1962). The scales were
administered before significant remission of symptoms, during the week in which patients were asked to keep a dream diary, which usually began upon admission. The mean score obtained in HAM-D (277 5.74) suggests severe depression in our sample. All patients scored between 5 and 7 on the “unusual thought content” item of the BPRS and presented with guilt, persecution, ruin and somatic delusions. 2.3. Pharmacotherapy None of the patients included in the study were drug-naïve; administration of treatment began at the moment of admission to our unit as prescribed by the assigned physician. Various combinations of antidepressants (all patients were treated with SSRIs), antipsychotics and benzodiazepines were administered to all patients during the week in which the material for the study was collected. 2.4. Study design All participants were asked to sign an informed consent to take part in the study. During the first week of hospitalization, patients were instructed to keep a dream diary where they could report each morning the dream they had had the night before. As instruction, participants were asked to report the whole development of the dream plot whenever possible. The material was always collected during the first week of hospitalization, before significant remission of the psychotic symptoms, whereas the control population completed dream diaries in their home setting. Subjects who successfully reported at least one dream were then administered a projective test used to elicit fantasy stories. The Thematic Apperception Test (TAT) consists of a broad set of figures, differentiated into groups of 20 according to sex and age (Murray, 1943). Seven figures chosen progressively from the full set were used in this study according to a previously published scheme (Scarone et al., 2008; Limosani et al., 2011; D’Agostino et al., 2012). Given that several authors have questioned the reliability and validity of the test's psychometric properties (Cramer, 1999), the TAT was only used in this study design to elicit waking fantasies from a standardized set of stimuli. All participants were asked to create a fantasy story that clearly contained a beginning, a plot development and an end based on the visualized figure after having eliminated the stimulus; the narratives created in response to the fixed stimulus were tape-recorded and then transcribed. 2.5. Formal analysis of narratives A total of 65 dream reports (25 belonging to depressed patients and 40 belonging to the control group) and 168 waking fantasy reports (84 for each group) were collected for analysis. The material was equally divided and randomly assigned to two judges who had no acquaintance with the study participants and were blind to the diagnosis and to the origin of the narrative transcripts. The Dream Bizarreness scale (Hobson et al., 1987) was used to score the material as described elsewhere (Scarone et al., 2008, Limosani et al., 2011). The following indices were calculated for each dream and TAT response: bizarreness intensity (BI), calculated as the number of bizarre events in the domains of plot, cognition, and affect, and bizarreness density (BD), calculated by dividing BI by the report word count. The following indices were then calculated for each subject, yielding normally distributed data: Bizarreness Density Index for dreams (BDI), calculated as the mean of the dream BD indices, and Bizarreness Density Index for TAT tables (BDI), calculated as the mean of the TAT table BD indices. 2.6. Dream content analysis The Hall/Van de Castle scoring system was used to analyse dream contents (Hall, Van de Castle, 1966). This scale is considered to be the most comprehensive and used empirical system for dream content analysis, with several nominal categories reflecting characters, aggressiveness, social interactions, emotions, etc. within the dream report (Domhoff, 1996). According to a previously published method, each content category was represented by a number reflecting the frequency of a given content within a dream report. An average index was developed for each participant based on the number of reported dreams. Scoring was undergone by one group-blind judge who was adequately trained in the use of the scale (Scarone et al., 2008; Limosani et al., 2011). 2.7. Statistical analyses All data analyses were performed with SPSS version 19.0 (IBM, 2010). Two-way Analysis of Variance (ANOVA) for repeated measures was applied to assess the effect of diagnosis and experimental study conditions (TAT stories and dream reports) on cognitive bizarreness. Pearson's correlation coefficient was used to measure the strength of the linear relationship between HAM-D-21 total score and BDI scores in the patient sample. Analysis of Variance (ANOVA) was applied to assess the effect of diagnosis on the content scored in dream reports using the Hall/
S. Cavallotti et al. / Psychiatry Research 216 (2014) 31–36 Van de Castle system. Content categories were treated as dependent variables with diagnosis as the fixed factor.
3. Results 3.1. Bizarreness in dream and waking fantasy reports Fig. 1 shows the means of dream and TAT BDIs in depressed and normal subjects. The interaction between the experimental conditions and diagnosis was highly significant (F1,20 ¼18.35, po0.01). Depressed patients had similar levels of cognitive bizarreness in their dream (BDI: M¼ 0.024, S.D.¼0.02) and waking (BDI: M¼0.025, S.D.¼0.01) mentation, whereas control subjects had a higher level in dreams (BDI: M¼0.038, S.D.¼0.01) and almost no bizarreness in wakefulness (BDI: M¼0.009, S.D.¼ 0.01). Independent-samples t-tests were conducted to compare BDI values in the two samples
Fig. 1. Mean BDI values in the wakefulness and dreams of patients diagnosed with PMD and healthy control subjects.
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across experimental conditions. Dream bizarreness was found to be significantly lower in the PMD group compared to the control group (t(20)¼2.83, po0.05). Within the control group, dream bizarreness was found to be significantly higher than waking bizarreness (t(20)¼ 7.99, po0.01). Finally, no significant difference could be found between dream and waking bizarreness bizarreness within the PMD group (t(20)¼ 0.18, p¼n.s.). Within the patient group, no correlation could be found between dream BDI and HAM-D-21 total score (r ¼ 0.41, p ¼n.s.) nor between BDI and HAM-D-21 total score (r ¼0.17, p ¼n.s.).
3.2. Length of reports and dream content Dream report length was found to be shorter in depressed individuals (M¼96.7, S.D.¼80) than in the healthy control population (M¼147.7, S.D.¼79). An independent-samples t-test conducted to compare dream report lengths in the two samples yielded no significant difference: t(20)¼ 1.5, p¼ 0.993. Therefore, no specific correction was necessary for content analysis. TAT reports were generally shorter than dream reports in both groups (Depressed subjects: M¼39.09, S.D.¼11.25; Control subjects: M¼56.3, S.D.¼32.2). An independent-samples t-test was conducted to compare TAT report lengths in the two samples. The observed difference was found to be statistically significant: t(20)¼ 1.67, po0.05. Fig. 2 shows the means of the indexes which refer to each content category scored with the Hall/Van de Castle system in depressed patients and normal controls. ANOVA yielded a significant Between-groups effect for three specific variables: Happiness (HA) (F1,21 ¼ 4.43, po0.05), Apprehension (AP) (F1,21 ¼7.43, po0.05) and Dynamism (DYN) (F1,21 ¼10.34, po0.05). Whereas the first was relatively frequent in the dreams of depressed patients (HA: M¼0.21, S.D.¼ 0.33), it was never scored in the control group (HA: M¼0). On the contrary, the latter two recurred with lower frequency in the patient sample (AP: M¼ 0.12, S.D.¼0.21; DYN: M¼0.42, S.D.¼0.71) compared to the control group (AP: M¼ 0.65, S.D.¼0.61; DYN: M¼1.47, S.D.¼0.82).
Fig. 2. Dream content in patients diagnosed with PMD and healthy control subjects according to the Hall/van de Castle scoring system. between the two groups.
n
Statistically significant differences
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4. Discussion 4.1. Stability of cognition across wakefulness and dreams In terms of formal aspects of cognition, bizarreness was found to be surprisingly stable across waking fantasies and dreams in PMD inpatients. This finding suggests that acutely psychotic subjects have similar levels of cognitive bizarreness in dream reports and verbal reports elicited by the TAT. Hence, this cognitive pattern that has been supposed to reflect underlying neurofunctional modifications (Mamelak and Hobson, 1986) could also be considered a distinctive formal property of the waking cognitive organization of psychosis. Our preliminary results on PMD patients dovetail nicely with previous finding in schizophrenic (Scarone et al., 2008) and manic (Limosani et al., 2011) subjects with acute psychotic symptoms. However, as clearly shown in Fig. 1, dream and waking levels of bizarreness in PMD patients are intermediate between the high level of dream bizarreness and the very low level found in the waking fantasies of the control population. This confirms previous findings in non-psychotic depressed patients, where dream bizarreness was lower compared to that of healthy subjects (Beauchemin and Hays, 1996).
(Hobson, 2009; Stephan, Friston and Frith, 2009; Wiffen and David, 2009). This deficit sustains the subject's firm belief in the truthfulness of his experience, be it a dream in which his house resembles his childhood school or the delusional idea that his body has transformed into a mass of rotting organs. The formal construction of dreams and psychotic processes measured as bizarreness could reflect a common underlying neurobiological mechanism by which the brain/mind loses its ability to engage a logical relationship with the external environment in the processing of incoming information (Corlett et al., 2010). Several neurophysiological, neurochemical and cerebrofunctional patterns of activity suggest similarities between dreaming and psychosis. Overlapping findings in these two conditions have been discussed elsewhere (D’Agostino et al., 2012). Hyperactivation of the dopaminergic reward system has recently been proposed to play a central role in the generation of dreams (Perogamvros and Schwartz, 2012). The same type of brain activity is broadly accepted as a final common pathway of several disturbances that lead to psychosis (Howes and Kapur, 2009). Indeed, aberrant attribution of salience to one's own experience coupled with impaired elaboration of prediction errors dependent on a hyperactive dopaminergic system can explain most phenomenological features of both dreams and psychosis.
4.2. Relationship between cognitive bizarreness and psychosis Cognitive bizarreness reflects discontinuous, incongruous and vague transitions within a report comprising thoughts, emotions and narrative plot (Hobson et al., 1987; Stickgold et al., 1994). Although some data suggest that waking imagery can contain bizarre elements (Klinger and Cox, 1987; Kane et al., 2007; Klinger, 2008), or even that waking imagery can be more bizarre than dreaming (Reinsel et al., 1992; Wollman and Antrobus, 1986), most studies confirm that bizarre elements are more prevalent in dreams than in waking imagery (Williams et al., 1992; Cicogna et al., 2007; Scarone et al., 2008; Limosani et al., 2011; Kahan and LaBerge, 2011). Moreover, although “thin boundary” personality has been related to more bizarre dreams and daydreams than “thick boundary”, as a whole dreams were found to be more bizarre than daydreams across both personality types (Kunzendorf et al., 1997), further strengthening the common assumption that cognitive bizarreness is a distinguishing feature of dreams. It has been observed that the few studies in which waking mentation appeared to be more bizarre adopted a sensory restriction protocol that could have influenced findings (Hobson et al., 2000). Indeed, subjects were asked to report imaginative experiences in a condition of darkness and sound restriction that is known to trigger psychotomimetic symptoms in healthy volunteers within 15 min (Mason and Brady, 2009). The recurrence of bizarreness in the waking mentation of acute psychotic patients belonging to different diagnostic domains warrants a closer discussion of its meaning. This peculiar type of cognition was originally attributed to the loss of noradrenergic modulation of the cortex (Hartmann, 1973) or the spontaneous activity of the brain as a closed system in absence of environmental inputs and voluntary self-regulation mechanisms (Rechtschaffen, 1978; Antrobus, 1991). More recently, it was correlated to the ponto-geniculo-occipital waves that have been recorded when cholinergic hyperactivity triggers REM sleep in the absence of aminergic inhibition (Quattrochi et al. 1998). In terms of functional activation in this stage of sleep, where bizarreness has been found to be highest, recent findings suggest a relationship between dream bizarreness and the decrease in temporal coupling between executive and perceptual regions of the cortex (Corsi-Cabrera et al., 2003). In psychosis and dreams alike, the subject's inability to discern the origin of emotion and perception-related internal sources appears to reflect a deficit of self-monitoring mechanisms mediated by the frontal lobes
4.3. Emotional tone in PMD dreams In terms of content, relevant peculiarities could be identified within the emotional tone of dreams. Surprisingly, dreams of PMD patients reflected more Happiness and less Apprehension compared to those of the control population. Despite some controversy amongst researchers, it is generally accepted that negative emotions such as sadness and apprehension outweigh positive ones in the dreams of healthy subjects (Schredl and Doll, 1998). Previous studies in non-psychotic depressed patients all report an intensification of such imbalance that has been interpreted as proof of continuity in emotional tone within subjects in wakefulness and dreams (Schredl et al., 2009). Untreated patients have been found to report dreams with more depressive contents when awoken from REM stages in the latter part of the night (Agargun and Cartwright, 2003) and the spontaneous dream recall upon awakening used in our protocol is generally thought to reflect the most recent oneiric episode of the night. The inversion of this balance in the dreams of patients with PMD could be interpreted as evidence of a pronounced affective dysregulation across the sleep/wake cycle in this population. Indeed, PMD has been found to be characterized by more severe REM sleep abnormalities when compared to non-psychotic depression (Thase et al., 1986). Although REM sleep is thought to promote consolidation of emotionally salient memories (Nishida et al. 2009), no speculations can be made on the basis of our findings given that sleep stage was not controlled. One other possible explanation of our finding is that positive dream emotions depend on the patients' antidepressant medication (see following section for a full discussion on the effect of psychotropic drugs on sleep and dreams). Indeed, one previous study found dream emotion to improve during the course of treatment with tricyclic antidepressant trimipramine (Schredl et al., 2009). However, previous findings suggest that dream emotion improvement parallels clinical improvement in nonpsychotic depressed patients, whereas our population presented severe depression with psychotic symptoms at the time of dream collection. More intuitively, the reduced Dynamism observed in the dreams of PMD patients can be interpreted as continuous with the typical psychomotor retardation of depressive syndromes.
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4.4. Methodological issues
References
Several limitations should be considered in discussing these preliminary results. First of all, enroled patients were on treatment with psychoactive drugs which might have influenced both the form and content both of dreams and waking fantasies. Dream recall frequency is known to decrease in depressed patients treated with all classes of antidepressant drugs, independent of drug-specific effects on REM sleep (Schredl et al., 2009). Antidepressant drugs could also influence the emotional tone of dreams. Available data are often contradictory and some authors report increased positive dream content associated with improvement in clinical symptoms (Schredl et al., 2009), whereas others describe no changes in dream content despite clinical improvement (Armitage et al., 1995). According to a recent review, the most consistent findings are that tricyclic antidepressants induce more positive dream emotions and that Selective Serotonin Reuptake Inhibitors (SSRIs) have a dream intensifying effect and may elicit more dream material (Tribl et al., 2012). In this study, all patients were treated with SSRIs that are known to suppress REM sleep (Wilson and Argyropoulos, 2005). Most patients were also treated with variable doses of benzodiazepinic agents that are also known to suppress both Slow Wave Sleep and REM sleep (Achermann and Borbély, 1987; Borbély et al., 1985; Gaillard et al., 1973) This may at least in part account for the intermediate levels of bizarreness found in their dreams. Regarding antipsychotic medications, it should be noted that the influence of these molecules on REM–NREM sleep architecture are still inconclusive (Nofzinger and Keshavan, 2002). A second relevant issue in our design is the lack of a control group of patients diagnosed with Major Depression without Psychotic features. Indeed, the present study design cannot exclude that observed levels of cognitive bizarreness depend on the depressive state rather than psychotic symptoms. Although bizarreness has been found to diminish in the dreams of depressed patients (Beauchemin and Hays, 1996), no previous studies analysed its expression during wakefulness in this population. Future studies with a three-group design will help to at least partially control for the effect of both medication and specific mood disorder on the results. A third issue that limits our findings regards the small sample of patients enroled in the study and the low number of dreams analysed.
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4.5. Conclusive remarks In conclusion, the present preliminary study appears to suggest that cognitive bizarreness can adequately measure the stability of cognition across dreams and wakefulness in acutely psychotic inpatients. With specific reference to PMD, dream content was found here to be surprisingly more positive in terms of emotional tone when compared to that of the general population and of previous reports in nonpsychotic depressed patients. This intriguing finding warrants further investigation and could reflect a discontinuity with waking emotion in these subjects.
Role of funding source None.
Acknowledgements The authors would like to thank Drs. Ivan Limosani and Maria Laura Manzone for their helpful discussions and their contribution to recruitment of control subjects.
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