This placebo-controlled study (n=56) investigated the acute effect of psilocybin (15mg/70kg) on empathy and moral decision-making in healthy human subjects. The results found the first such evidence that psilocybin has distinct effects on social cognition by enhancing emotional empathy but not moral behavior. It also supports previous findings, indicating that psilocybin may promote emotional empathy presumably through activation of serotonin 2A/1A receptors, showing that focusing on serotonin 2A/1A receptors has the potential to treat dysfunctional social cognition.
Background
Impaired empathic abilities lead to severe negative social consequences and influence the development and treatment of several psychiatric disorders. Furthermore, empathy has been shown to play a crucial role in moral and prosocial behavior. Although the serotonin system has been implicated in modulating empathy and moral behavior, the relative contribution of the various serotonin receptor subtypes is still unknown.
Methods
We investigated the acute effect of psilocybin (0.215 mg/kg p.o.) in healthy human subjects on different facets of empathy and hypothetical moral decision-making using the multifaceted empathy test (n=32) and the moral dilemma task (n=24).
Results
Psilocybin significantly increased emotional, but not cognitive empathy compared with placebo, and the increase in implicit emotional empathy was significantly associated with psilocybin-induced changed meaning of percepts. In contrast, moral decision-making remained unaffected by psilocybin.
Conclusions
These findings provide first evidence that psilocybin has distinct effects on social cognition by enhancing emotional empathy but not moral behavior. Furthermore, together with previous findings, psilocybin appears to promote emotional empathy presumably via activation of serotonin 2A/1A receptors, suggesting that targeting serotonin 2A/1A receptors has implications for potential treatment of dysfunctional social cognition.
Papers cited by this study that are also in Blossom
Bernasconi, F. ;., Schmidt, A. ;., Pokorny, T. ;. et al. · Cerebral Cortex (2013)
Carter, O. L., Hasler, F. ;., Pettigrew, J. D. et al. · Psychopharmacology (2007)
Dolder, P. C., Schmid, Y., Müller, F. et al. · Neuropsychopharmacology (2016)
Geyer, M. A., Vollenweider, F. X. · Trends in Pharmacological Sciences (2008)
Empathy and moral behaviour are central to social functioning and are implicated in several psychiatric disorders. Empathy is described as having at least two components: cognitive empathy (understanding another's mental state, akin to Theory of Mind) and emotional empathy (sharing another's emotional state). Deficits in these domains are reported in conditions such as major depressive disorder, bipolar disorder, borderline personality disorder and psychopathy, and may worsen with illness progression. Moral decision-making is commonly studied using hypothetical moral dilemmas that pit utilitarian outcomes against deontological constraints; personal dilemmas that involve directly harming another person are more emotionally engaging and tend to elicit deontological responses. Serotonin (5-HT) has been implicated in both empathy and moral processes, but the specific contributions of different 5-HT receptor subtypes remain unclear. Previous pharmacological work showed that MDMA increases emotional but not cognitive empathy, and that manipulating 5-HT tone with SSRIs can increase harm aversion in moral judgements, suggesting receptor-specific effects worth clarifying. Pokorny and colleagues set out to test the acute effects of psilocybin — a serotonergic hallucinogen acting primarily at 5-HT2A and also 5-HT1A receptors — on multiple facets of empathy and on hypothetical moral decision-making in healthy volunteers. The principal hypotheses were that psilocybin would impair cognitive empathy for negative stimuli while increasing emotional empathy, and that it would reduce utilitarian choices in personal moral dilemmas. The study therefore examined cognitive empathy, explicit and implicit emotional empathy using the Multifaceted Empathy Test (MET), and moral choice behaviour using a moral dilemma task (MDT), in a double-blind, placebo-controlled, within-subject design.
Thirty-three healthy volunteers were recruited; after exclusions one participant was removed for failing to understand the MET, leaving 32 participants (17 men, 15 women; mean age 26.72 ± 5.34 years) for the MET analyses. The MDT was implemented later and completed by 24 participants (13 men, 11 women; mean age 26.63 ± 5.33 years). Eligible participants were aged 20–40, screened by physical exam, ECG, blood and urine tests (including drug screen and pregnancy test), and structured psychiatric interviews to exclude current or past neurological or psychiatric disorders and first-degree relatives with major psychiatric illness. Participants agreed to abstain from illicit drugs for at least 2 weeks prior to and during the study. The study used a double-blind, randomised, placebo-controlled, within-subject cross-over design with two sessions separated by at least 10 days. Each participant received oral psilocybin at 0.215 mg/kg in one session and matched placebo capsules (mannitol) in the other. Tasks (MET and MDT) were administered on a computer in a quiet room 160 minutes after ingestion, when the peak perceptual effects had largely subsided. Subjective effects were assessed with the 5D-ASC (5-Dimensional Altered States of Consciousness) at 360 minutes post-dose and mood with the Positive and Negative Affect Schedule (PANAS) before and 360 minutes after dosing. Participants were monitored by a physician until effects resolved. Measures: Trait empathy was assessed once at screening with the Interpersonal Reactivity Index (IRI). The MET (40 photos; 20 positive, 20 negative) yielded cognitive empathy (identify the emotion from four choices), explicit emotional empathy (self-rated concern or happiness on a 9-point scale), and implicit emotional empathy (self-rated arousal on a 9-point scale). The MDT comprised two matched sets of 22 vignettes including personal (avoidable and inevitable), impersonal and nonmoral dilemmas; responses were binary choices of utilitarian action versus harm avoidance. The 5D-ASC provided multiple subscale scores including changed meaning of percepts. PANAS measured positive and negative affect and seven arousal-related items. Statistical approach: Repeated-measures ANOVAs tested drug (psilocybin, placebo) and valence or dilemma category as within-subject factors, with order (placebo first, psilocybin first) as a between-subjects factor. ANCOVAs controlled for mood changes where relevant. Paired t tests compared nonmoral scenario accuracy between conditions. Regression analyses (backward stepwise) examined whether 5D-ASC scales, PANAS change scores, or IRI subscales predicted empathy changes; moderator analyses tested whether arousal moderated relationships. Analyses used a significance threshold of P < .05 (two-tailed). PANAS data were missing for one participant and noted as such.
Subjective effects and mood: Psilocybin produced robust alterations on the 5D-ASC, with a significant drug by scale interaction (F(10,310) = 25.06, P < .0001) and a main effect of drug (F(1,31) = 100.66, P < .0001). Posthoc tests showed that psilocybin increased all 5D-ASC scale scores relative to placebo except for anxiety. On the PANAS there was a drug × time × scale interaction (F(1,30) = 6.58, P < .05) and a drug × time interaction (F(1,30) = 17.34, P < .001); positive affect increased under psilocybin (P < .05) while negative affect did not change. Arousal increased under psilocybin (psilocybin mean = 0.25, SD = 0.39) relative to placebo (mean = -0.07, SD = 0.32; t(31) = -3.96, P < .001). MET outcomes: For explicit emotional empathy there was a significant main effect of drug (F(1,30) = 7.74, P < .01), with higher ratings under psilocybin than placebo; this effect did not interact with stimulus valence. Implicit emotional empathy was also increased by psilocybin (F(1,30) = 4.77, P < .05), again without a valence interaction. Cognitive empathy showed no significant main effect of drug (F(1,30) = 1.45, P > .2), indicating no psilocybin-induced impairment in identifying others' emotions. A valence main effect indicated more errors for negative versus positive stimuli (F(1,30) = 6.58, P < .05). Results remained broadly unchanged when controlling for positive or negative mood, except implicit emotional empathy lost significance when controlling for positive mood (F(1,30) = 2.62, P > .11). No differences were found between psilocybin-experienced and psilocybin-naïve participants on MET scores in the psilocybin condition. Associations: Multiple regression showed that 5D-ASC scales explained a significant portion of variance in the psilocybin-induced increase in implicit emotional empathy (F(1,31) = 11.23, P < .01; R2 = .27), with the changed meaning of percepts subscale as the sole significant predictor (Beta = .52, t(31) = 3.35, P < .01). Moderator analyses testing arousal as a moderator found that arousal did not significantly predict implicit emotional empathy nor moderate the relationship between changed meaning of percepts and implicit emotional empathy; the key predictor remained changed meaning of percepts. Trait empathy (IRI) and PANAS change scores did not significantly predict empathy increases in these models. MDT outcomes: No drug effects emerged on moral decision-making. There was no significant drug × category interaction (F(2,44) = 0.97, P > .3) and no main effect of drug on the proportion of utilitarian choices (F(1,22) = 0.37, P > .5). However, participants made more incorrect responses on nonmoral dilemma scenarios under psilocybin (placebo mean = 0.99, SD = 0.05; psilocybin mean = 0.91, SD = 0.16; t(23) = 2.98, P < .01), though the absolute error rate under psilocybin was low (about 9%). Including mood covariates did not alter the MDT results, and no differences emerged between psilocybin-experienced and naïve participants on MDT performance.
Pokorny and colleagues interpret the findings as evidence that a single moderate dose of psilocybin selectively enhances emotional empathy (both explicit concern and implicit arousal-related empathy) without altering cognitive empathy or hypothetical moral choice. The increase in implicit emotional empathy was associated with the 5D-ASC subscale changed meaning of percepts, which assesses heightened significance and emotional engagement with objects or surroundings; the authors suggest this altered sense of significance may also extend to perceiving and emotionally engaging with other people. Trait empathy did not predict the empathy enhancement, implying the effect may operate independently of baseline empathic disposition. Although psilocybin elevated arousal and positive affect, arousal did not statistically moderate the link between changed meaning of percepts and implicit emotional empathy, and mood changes did not account for most empathy effects, although implicit empathy lost significance when controlling for positive mood in one analysis. The authors situate these results within serotonergic receptor mechanisms: psilocybin's primary action at 5-HT2A receptors and partial modulation via 5-HT1A receptors might underlie the empathy enhancement. They note parallel findings with MDMA and LSD on emotional empathy and point out that prior MDMA work implicated 5-HT mechanisms but did not implicate 5-HT1A in MDMA's empathogenic effects; by contrast, psilocybin's combined 5-HT2A/1A action makes both receptor subtypes plausible contributors. The discussion also references neuroimaging work linking emotional empathy to regions such as the insula and amygdala and notes that psilocybin increases activity in frontomedial, frontolateral and temporal cortices and the insula, providing a possible neural substrate for increased emotional sharing. Regarding moral decision-making, the lack of effect on utilitarian choices is emphasised. The authors note that moral judgement and choice of action may be dissociable processes with different neural bases; prior SSRI work that increased harm aversion assessed moral judgement rather than action choice, which might explain divergent results. They also acknowledge alternative explanations: psilocybin might require higher doses to affect the networks underlying moral choices, or reduced emotional salience of personal dilemmas under psilocybin (via lowered amygdala or ACC responses) could obscure changes. The small increase in errors on nonmoral items under psilocybin might reflect mild attentional effects or tiredness given task order, and the authors concede such factors could have masked potential MDT effects. Limitations and implications discussed by the authors include that psilocybin acts at multiple 5-HT receptor subtypes so receptor-specific conclusions remain tentative; they call for studies combining psilocybin with selective antagonists to parse receptor contributions. The clinical relevance is highlighted cautiously: because emotional empathy is impaired in disorders such as depression and psychopathy, 5-HT2A/1A receptor agonists might have therapeutic potential for social cognition deficits, but further research is required. The authors also note that the empathy enhancement was not simply attributable to visual hallucinations or perceptual disturbances, given the lack of association with visual hallucination measures.
Data were analyzed using STATISTICA 8.0 for Windows (StatSoft). For the MET, repeated-measures ANOVAs were computed to analyze data of each empathy component (cognitive empathy, explicit emotional empathy, implicit emotional empathy) with drug (psilocybin, placebo) and valence (positive stimuli, negative stimuli) as within-subject factors and order (placebo first, psilocybin first) as between-subjects factor. For the MDT, the ratio of utilitarian choice (amount of utilitarian answers/total questions) for each category was computed, and a repeated-measures ANOVA was conducted to analyze the ratio of utilitarian choices with moral dilemma category (personal avoidable dilemma, personal inevitable dilemma, impersonal dilemma) and drug (psilocybin, placebo) as within-subject factors and order (placebo first, psilocybin first) as between-subjects factor. To compare the ratio of correct answers in nonmoral dilemma scenarios between the placebo and psilocybin condition, a paired t test was conducted. To control for psilocybin-induced mood changes on the scores of the MET and MDT, ANCOVAs with changes scores (post minus pre psilocybin condition) of positive affect and negative affect from the PANAS as covariates were performed. Independent-samples t tests were performed between psilocybin-experienced (n = 10) and psilocybin-naïve (n = 22) participants to compare their MET and MDT scores in the psilocybin condition. A repeated-measures ANOVA with drug (psilocybin, placebo) and 5D-ASC scale scores (experience of unity, spiritual experience, blissful state, insightfulness, disembodiment, impaired control and cognition, anxiety, complex imagery, elementary imagery, audio-visual synesthesiae, changed meaning of percepts) as within-subject factors were computed for the 5D-ASC ratings. A repeated-measures ANOVA with drug (psilocybin, placebo), time (pre, post), and scale scores (positive affect, negative affect) as within-subject factors were computed for the PANAS scores. Tukey posthoc comparisons followed significant main effects or interactions in the ANOVAs. In case of significant drug effects on outcome measures, change scores were computed (psilocybin minus placebo). To test the potential role of increased arousal on significant outcome measures, an arousal change score (post minus pre drug administration) from the mean of the 7 arousal-related PANAS itemswas computed. A moderator analysis was conducted to ascertain whether the relationship between changed meaning of percepts change scores and implicit emotional empathy change scores is influenced by arousal. To represent the interaction between changed meaning of percepts and arousal, the variables were first centered and then multiplied together. PANAS scores of one subject could not be analyzed due to missing data. Finally, the potential effects of altered states of consciousness (5D-ASC scales change scores), mood change (PANAS post minus pre psilocybin condition), and trait empathy (IRI subscales) on significant outcome measures were explored by means of multiple regression analyses using the backward stepwise method. The confirmatory statistical comparisons of all data were carried out on a significance level set at P < .05 (2-tailed).
Psilocybin significantly increased explicit and implicit emotional empathy independent of stimuli valence. The increase in implicit emotional empathy was related to alterations in meaning of percepts but not trait empathy. There was no significant change in cognitive empathy between placebo and psilocybin. Although psilocybin led to an increase of emotional empathy, no significant difference in decision-making on hypothetical moral dilemmas was found between placebo and psilocybin. The present finding suggests that 5-HT2A and 5-HT1A receptor systems may be important in the experience of emotional empathy regardless of the emotional valence of the stimuli. Interestingly, previous work has shown that psilocybin modulates the processing and recognition of negative social and nonsocial stimuli, presumably via 5-HT2A and/or 5-HT1A receptor activation. Specifically, it has been shown that activation of 5-HT2A receptors is implicated in early encoding and recognition of negative facial expressions, whereas the 5-HT1A receptor activation seems to influence later processing of both negative and positive facial expression. Taken together, the present results extend these findings and suggest that the 5-HT2A receptor and possibly also the 5-HT1A receptor are not only implicated in the processing of social and nonsocial emotional stimuli but that they may also be involved in sharing the emotional state of another person (implicit emotional empathy) and the experience of sympathy and prosocial attitudes towards others (explicit emotional empathy). Furthermore, cognitive empathy remained unaffected by psilocybin, indicating that participants completed the task attentively and correctly. In contrast to emotional empathy, which measures one's current experience of the emotional state of another person, cognitive empathy/Theory of Mind requires the ability to correctly identify the other person's emotions. It is possible that emotional empathy in contrast to cognitive empathy is dependent on state variables and may therefore be manipulated more easily whereas it probably takes more time to acquire new cognitive empathy skills. The 5D-ASC scale score changed meaning of percepts assesses a change in the significance of objects or the surroundings and significantly predicted the increase in implicit emotional empathy scores in the psilocybin condition. Some items of this 5D-ASC scale also refer to a change in the relationship between the observer and the observed objects or the environment. This is reflected for example by the item "Objects around me engaged me emotionally much more than usual". Such an increased emotional engagement seems to be reflected in the boosted implicit emotional empathy ratings in the present study, indicating that the increased sense of significance may not solely refer to surrounding objects but also to the emotional state of other persons. Although psilocybin significantly increased participant's arousal scores on the PANAS, the relationship between implicit emotional empathy and changed meaning of percepts was not moderated by arousal. It is noteworthy that the acute mood enhancing effects of psilocybin did not significantly predict the increase in emotional empathy. However, as there was no significant drug effect on implicit emotional empathy when controlling for psilocybin-induced positive affect, we cannot rule out that positive mood was associated with increases in implicit emotional empathy. The psilocybin-induced enhancement of emotional empathy was also not significantly predicted by the trait empathy score of the IRI questionnaire, suggesting that the acute empathy enhancing effect of psilocybin may build up independently from the subject's baseline or trait empathy level. While the IRI scores in our study sample are comparable with scores from a meta-analysis investigating US college students from 1980 to 2009, the finding that psilocybin's empathy enhancing effect is independent from trait empathy might be especially relevant for the treatment of psychiatric disorders where the affected patient has low trait empathy levels such as in psychopathy. In line with this idea studies in the 1960s suggested that psychedelics such as psilocybin and LSD might be useful in the treatment of psychopaths and criminals. Finally it is noteworthy that the implicit and explicit emotional empathy ratings were not associated with the psilocybin-induced visual illusions and hallucinations suggesting that the empathy enhancement is not simply based on visual inaccuracy or disturbances. A recent fMRI study using the MET showed that emotional empathy in healthy subjects is associated with increased BOLD responses in the brainstem, inferior frontal cortex, posterior superior temporal sulcus, temporal lobe, posterior insular cortex, and posterior cingulate cortex. Whereas prefrontal areas seem to be specifically related to simulating the perspective of others and stepping into their shoes, regions such as the insula and amygdala appear to be important for enabling the experience of emotional empathy. Given that psilocybin increased neuronal activity as indexed by cerebral glucose metabolism or cerebral blood flow in frontomedial and frontolateral cortices including the anterior cingulate cortex (ACC), the temporomedial cortex, the insula, and the basal gangliait is conceivable that psilocybin may increase emotional empathy via activation of frontal-temporal and subcortical structures. The present findings on the effects of psilocybin in the MET endorse the importance of the 5-HT system in empathy. Similar effects were found in previous studies investigating the influence of the 5-HT releasing agent MDMA on the same task. Specifically, MDMA significantly increased explicit and implicit emotional empathy for all stimuli. It is noteworthy that neither oxytocin nor pretreatment with the 5-HT1A receptor antagonist pindolol modulated the empathogenic effects of MDMA. Moreover, a recent study showed that LSD, which acts as an agonist at multiple 5-HT and dopamine receptor sites, dosedependently increased explicit and implicit emotional empathy, but in contrast to the present findings with psilocybin, LSD in addition impaired cognitive empathy. As the psychological effects of psilocybin are primarily mediated via 5-HT2A receptor activation and partially modulated by 5-HT1A receptor manipulations, both these 5-HT receptor sites may be crucially implicated in the generation of emotional empathy. However, given that psilocybin acts also on other 5-HT receptor subtypes, further psilocybin studies in combination with selective 5-HT receptor antagonists are warranted to examine the relative contribution of specific 5-HT receptor subtypes on empathy. Although psilocybin also has downstream effects on the dopamine system, an involvement of the dopamine system in the current results is unlikely since administration of the dopamine reuptake inhibitor methylphenidate did not lead to increased empathy ratings in the MET. Whereas psilocybin increased emotional empathy, it did not affect moral decision-making in any dilemma condition in the MDT. Neuroimaging studies revealed that moral decision-making and empathy are mediated by overlapping networks, but they also have distinct neuronal correlates. Our finding is well in line with the observation that the serotonin-releasing agent MDMA increased emotional empathy but had no effects on moral judgment in moral dilemma tasks. Further, a metaanalysis of fMRI and PET studies investigating the relationship between morality and empathy revealed that affective sharing is unlikely involved during moral decisions. However, our finding is somewhat surprising given that manipulating the serotonergic tone by a single dose of the serotonin reuptake inhibitor citalopram was reported to lead to harm avoidance in the judgment of personal moral dilemmasand to an aversion for painful electric shocks for oneself and others. However this apparent discrepancy may be explained by the fact thathad examined moral judgments ("Is it acceptable to…?"), whereas we investigated moral decision-making with a choice of action ("Would you…?") condition. A recent study investigating whether evaluative judgments and choices of action differ when people make decisions on dilemmas involving moral issues suggests that judgment and choice of action are mediated, at least in part, by distinct psychological processes, which in turn rely on different neural underpinnings. Specifically, using identical dilemma tasks it has been suggested that moral judgment is linked to the functional integrity of the right dorsolateral prefrontal cortex, whereas moral action choice may mainly rely on ventromedial prefrontal cortex function. Taken together, these findings and the dissociable effects of psilocybin on empathy and choice of action suggest that the 5-HT2A/1A receptor system may not be involved in moral decision-making. However, it may also be possible that higher doses of psilocybin are needed to alter the functional integrity of the neuronal networks underlying social moral decisions and choices of action. Furthermore, it is also noteworthy that personal moral scenarios involve emotionally salient violent acts. Such scenarios activate brain regions implicated in emotional processing, including visual pathways and the amygdala. Psilocybin has been shown to reduce the neuronal response to social exclusion in the ACCand to lead to a decreased amygdala reactivity to threatening stimuli. Thus, it is possible that emotionally loaded personal moral scenarios were less emotionally salient in the psilocybin condition and therefore psilocybin did not enhance aversive emotional reactions to harm others as it was found with citalopram. Although participants made significantly more errors in nonmoral dilemmas under psilocybin than under placebo, the error rate in the psilocybin condition (9%) remained very low as well. We are therefore confident that participants could complete the task after psilocybin administration. However, we cannot rule out that this increase could be due to tiredness, as the task was run as the last test of the session. Therefore, it is possible that deficits in attention may have masked potential effects in the MDT. In conclusion, whereas moral decision-making was unaffected by psilocybin, the results from the MET indicate that psilocybin enhances emotional empathy but not the cognitive component of empathy. This finding highlights the possible role of 5-HT2A/1A receptors in everyday social experience. Therefore, 5-HT2A/1A receptor agonists may have potential beneficial effects in the treatment of mood disorders or psychopathy, which are characterized by deficits in social skills and in particular in the ability to feel with other people.
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