This double-blind, placebo-controlled, within-subjects study (n=50) investigated the psilocybin-induced spiritual experiences and insightfulness in healthy humans to understand the state of consciousness-related neuronal mechanisms using high-density electroencephalogram (EEG) recordings. The results identified a correlation between the intensity levels of psilocybin-induced spiritual experience and EEG measures. The study proposed that the identified mechanism may help find a way for modulating mental health considering that spiritual experiences improve well-being and psychological resilience.
Rationale
During the last years, considerable progress has been made toward understanding the neuronal basis of consciousness by using sophisticated behavioral tasks, brain-imaging techniques, and various psychoactive drugs. Nevertheless, the neuronal mechanisms underlying some of the most intriguing states of consciousness, including spiritual experiences, remain unknown.
Objectives
To elucidate state of consciousness-related neuronal mechanisms, human subjects were given psilocybin, a naturally occurring serotonergic agonist and hallucinogen that has been used for centuries to induce spiritual experiences in religious and medical rituals.
Methods
In this double-blind, placebo-controlled study, 50 healthy human volunteers received a moderate dose of psilocybin, while high-density electroencephalogram (EEG) recordings were taken during eyes-open and eyes-closed resting states. The current source density and the lagged phase synchronization of neuronal oscillations across distributed brain regions were computed and correlated with psilocybin-induced altered states of consciousness.
Results
Psilocybin decreased the current source density of neuronal oscillations at 1.5-20 Hz within a neural network comprising the anterior and posterior cingulate cortices and the parahippocampal regions. Most intriguingly, the intensity levels of psilocybin-induced spiritual experience and insightfulness correlated with the lagged phase synchronization of delta oscillations (1.5-4 Hz) between the retrosplenial cortex, the parahippocampus, and the lateral orbitofrontal area.
Conclusions
These results provide systematic evidence for the direct association of a specific spatiotemporal neuronal mechanism with spiritual experiences and enhanced insight into life and existence. The identified mechanism may constitute a pathway for modulating mental health, as spiritual experiences can promote sustained well-being and psychological resilience.
Papers cited by this study that are also in Blossom
Carhart-Harris, R. L., Erritzoe, D., Williams, T. et al. · PNAS (2012)
Griffiths, R. R., Richards, W. A., Mccann, U. et al. · Journal of Psychopharmacology (2006)
Griffiths, R. R. · Journal of Psychopharmacology (2008)
Grob, C. S., Bossis, A. P., Griffiths, R. R. · Preprints (2013)
Spiritual experiences are rare but salient states of consciousness that can promote sustained well-being and resilience, yet their neuronal correlates remain poorly understood because such experiences are infrequent and unpredictable. Earlier research has focused largely on traits that predispose individuals to transcendent experiences, and recent placebo-controlled pharmacological studies have shown that the serotonergic hallucinogen psilocybin can dose-dependently elicit profound spiritual experiences, unity, insightfulness and bliss. Neuronal oscillations and their phase synchronization are proposed mechanisms of neuronal integration that shape conscious states; previous animal and human work with serotonergic hallucinogens (and related preparations such as ayahuasca/DMT) has suggested decreases in low-frequency oscillatory power, particularly in the alpha band, but whether oscillatory power or interregional phase relationships specifically underpin spiritual experiences is unresolved. This study by Kometer and colleagues set out to characterise how psilocybin alters the spatial distribution of neuronal oscillatory power and the dynamic coordination of oscillations across brain regions, and to test whether these electrophysiological changes correlate with psilocybin-induced spiritual experiences and insightfulness. Using a double-blind, placebo-controlled, within-subject design in healthy volunteers, the investigators recorded high-density EEG during eyes-open and eyes-closed resting states, computed intracerebral current source density and lagged phase synchronization across frequency bands, and related these measures to scores on the validated 5D-ASC questionnaire assessing altered states of consciousness.
Fifty-five healthy volunteers were recruited and screened by physical exam, electrocardiography, blood analyses, psychiatric interviews and urine drug testing; five were excluded for EEG-artifact contamination, leaving 50 participants (28 males, 22 females; mean age 24.8 ± 4.0 years) for analysis. The study pooled data from three parallel double-blind, placebo-controlled, within-subject pharmacological studies in which each participant completed four sessions (placebo+placebo, placebo+psilocybin, drug1+placebo, drug1+psilocybin) with sessions separated by at least 2 weeks. For the present analyses only the two placebo-controlled sessions (placebo+placebo and placebo+psilocybin) were used. Psilocybin doses were moderate: 170 μg/kg p.o. for most subjects and 215 μg/kg p.o. in one subgroup, administered 1 hour after the first capsule; the choice of moderate dosing was motivated in part by the need to minimise facial-muscle artefacts in the EEG. EEG was recorded from 64 scalp electrodes (BioSemi ActiveTwo) at 512 Hz in a shielded room 60 minutes after administration. Resting-state recordings comprised eyes-open (gaze fixed on a central cross) and eyes-closed conditions, presented in randomised order; each eyes condition lasted 2 min in study 1 and 2.5 min in studies 2–3. Vigilance was monitored and investigators intervened if strong drowsiness appeared. Subjective effects were measured after drug effects subsided using the 5D-ASC questionnaire (11 subscales including spiritual experience, experience of unity, insightfulness and blissful state). EEG preprocessing included filtering (low cutoff 0.5 Hz), removal of ocular and muscle artifacts via infomax ICA, interpolation of bad channels, average re-reference, segmentation into 2-s epochs and visual inspection to remove residual artefacts. Mean artifact-free epoch counts per condition were reported (≈116–124 epochs) and did not differ significantly between drug or eyes conditions. eLORETA source localisation was applied to compute three-dimensional intracerebral current density across 6,239 voxels (5×5×5 mm resolution) restricted to cortical grey matter and hippocampus. Eight frequency bands were analysed: delta (1.5–4 Hz), theta (4–8 Hz), alpha1 (8–10.5 Hz), alpha2 (10.5–13 Hz), beta1 (13–20 Hz), beta2 (20–30 Hz), gamma1 (30–45 Hz), and gamma2 (55–100 Hz). Voxel-wise dependent t tests compared current source density between placebo and psilocybin for each band and condition, with 5,000 permutations used to estimate the empirical null distribution and correct for multiple comparisons. Interregional coordination was assessed via lagged phase synchronization computed in eLORETA source space. Lagged phase synchronization quantifies the phase relationship between two regions after removing zero-lag contributions, thereby reducing volume-conduction and instantaneous-artifact confounds; the analysis used centroids of 42 Brodmann areas per hemisphere as regions of interest and calculated pairwise lagged phase synchronization across all ROI pairs for each frequency band and eyes condition. Dependent-samples t tests with 5,000 permutations corrected for multiple comparisons were used to test drug effects on lagged phase synchronization, and product-moment correlations (with permutation-based thresholding) related lagged phase synchronization values in the psilocybin condition to the 11 5D-ASC subscale scores.
Subjective effects: Repeated-measures ANOVA on 5D-ASC scores showed a robust main effect of drug (psilocybin vs placebo; F(1,48)=64.23, p<0.00001) and of subscale (F(10,480)=20.57, p<0.00001), with no significant main effect of dose (170 vs 215 μg/kg). Post hoc tests indicated that psilocybin significantly increased scores on all 11 subscales (all p<0.05), including spiritual experience, experience of unity, blissful state and insightfulness (all p<0.00001). Higher dose produced slightly higher scores on elementary hallucinations (p<0.05) and blissful state (p<0.01), but doses were overall similar. Current source density: In the eyes-closed condition psilocybin significantly decreased intracerebral current source density across oscillations from 1.5–20 Hz (p max = 0.00020, corrected), and in the eyes-open condition decreases extended up to 30 Hz (p max = 0.00020, corrected). The most consistent reductions in low-frequency power (<20 Hz) were localised to the posterior cingulate cortex (PCC; BA23/31) and the retrosplenial cortex (RSC; BA30), with additional decreases in the anterior cingulate cortex (ACC; BA24), precuneus (BA31), cuneus (BA30), parahippocampal gyrus (BA27/30) and other RSC areas (BA29). Theta and alpha1 band decreases were more widespread and included insula (BA13), occipitotemporal cortex (BA37) and parahippocampal regions (BA35/36). In the alpha1/alpha2 bands reductions covered large posterior occipital–parietal areas (BA7, BA17–19), especially on the right. There were no significant group-level effects in the gamma1 band (30–45 Hz). High-frequency oscillations (55–100 Hz) exhibited a psilocybin-induced increase in the left RSC (BA29) during eyes-closed (p max = 0.020, corrected) and a trend-level increase in RSC during eyes-open (p max = 0.054, corrected). Correlations between current source density and subjective state were limited. Only the insightfulness subscale correlated significantly with current source density in the alpha2 band (10.5–13 Hz) in very posterior medial parieto-occipital areas during the eyes-open condition; importantly, this region was not reduced by psilocybin at the group level, suggesting that intact alpha2 power in that posterior area related to higher insightfulness when other surrounding areas were reduced. No other 5D-ASC subscales showed significant correlations with current source density after correction. Lagged phase synchronization: Psilocybin produced a small increase in interhemispheric lagged phase synchronization of delta oscillations (1.5–4 Hz) during eyes-open, reaching significance between right BA7 and left BA39 (p max = 0.017, corrected); a trend was observed in eyes-closed (p max = 0.063, corrected). Crucially, within the eyes-closed condition the intensity of insightfulness and spiritual experiences correlated strongly and specifically with lagged phase synchronization of delta oscillations within a network of deep cortical structures. Insightfulness correlated with delta lagged phase synchronization between BA27–BA34, BA29–BA34, and BA28–BA47 (p max = 0.0028, corrected), while spiritual experience scores correlated with synchronization between BA28–BA29, BA34–BA29, and BA20–BA41 (p max = 0.029, corrected). The other nine 5D-ASC subscales showed no significant correlations with lagged phase synchronization in any frequency band (p max = n.s.), indicating specificity of these associations. Some reported effects reached only trend-level significance after correction.
Kometer and colleagues interpret their findings as evidence that psilocybin decreases ongoing lower-frequency oscillations (1.5–20 Hz), especially in theta/alpha bands, within an extended network centred on PCC, RSC, ACC and parahippocampal regions—areas that overlap substantially with the default-mode network (DMN). The investigators note that similar reductions in lower-frequency power have been observed with other serotonergic hallucinogens and that 5-HT2A receptor activation mediates decreases in alpha oscillations; they therefore propose that attenuation of ongoing lower-frequency oscillations, particularly in the DMN, may be a common action of serotonergic hallucinogens. The modest increase in high-gamma power in RSC is interpreted as consistent with an excitation/inhibition (E/I) shift toward excitation, and the authors suggest that disruption of lower-frequency rhythms may perturb the temporal structure of neuronal processing and thereby alter self-referential functions associated with the DMN, contributing to experiences such as unity. However, the authors emphasise that regional power decreases were only weakly associated with subjective reports: after correction, only insightfulness correlated with alpha2 power in a posterior parieto-occipital area during eyes-open. By contrast, lagged phase synchronization emerged as the stronger electrophysiological correlate of specific subjective states. The authors highlight that increased lagged phase synchronization of delta oscillations between parahippocampal areas, the RSC and lateral orbitofrontal cortex correlated with insightfulness and spiritual experience scores, and they link these regions and frequency band to autobiographical memory retrieval, memory valence attribution and coding of self-location within a global spatial context. From this perspective, insightfulness may reflect increased retrieval and reattribution of autobiographical memories, while spiritual experiences may involve a reorganisation of the self in a broader spatial context mediated by delta-phase coupling. The investigators stress the specificity of these associations: lagged phase synchronization correlations were observed for insightfulness and spiritual experiences but not for other psilocybin-induced phenomena (for example blissful state or disembodiment), and significant correlations were found primarily in the eyes-closed condition. They therefore suggest that eyes-closed resting-state paradigms may be particularly suitable for probing the neuronal mechanisms of these experiences and note that the identified network might be a pathway through which serotonergic modulation influences mental health. The authors refer to prior reports linking spiritual experiences with sustained well-being and to emerging therapeutic findings for psilocybin in mood disorders and anxiety in terminal illness, and they propose that future studies should test whether modulation of lagged phase synchronization among RSC, parahippocampus and lateral orbitofrontal cortex can promote mental health via autobiographical memory processes and changes in self-representation. The authors acknowledge limits inherent in the data: some effects were trend-level after correction, correlations were mostly confined to eyes-closed recordings, and the identified oscillatory changes alone were not sufficient to explain the full range of altered conscious states. They further note methodological choices such as using moderate psilocybin doses to reduce artefacts and restricting analysis to the placebo versus psilocybin sessions; these design features were intended to improve EEG data quality and the robustness of correlations but also shape the generalisability of findings. Overall, the discussion frames the results as providing systematic evidence that specific spatiotemporal neuronal mechanisms—namely decreased low-frequency oscillatory power within the DMN and increased delta-band phase synchronization across parahippocampal–retrosplenial–orbitofrontal networks—are associated with psilocybin-induced spiritual experiences and insightfulness.
Our data demonstrate that the serotonergic hallucinogen psilocybin decreased ongoing oscillations at 1.5-20 Hz within the PCC, the RSC, the anterior cingulate cortex (ACC), and parahippocampal regions during the resting state. This decrease was spatially most extended in the alpha and theta frequency bands and reached its maximum within the PCC, a key structure of the default-mode network. By contrast, high-frequency oscillations (55-100 Hz) within the RSC were slightly increased by psilocybin. Finally, and most interestingly, lagged phase synchronization of delta oscillations (1.5-4 Hz) within a network comprising the RSC, the parahippocampus, and the lateral orbitofrontal area were associated with spiritual experiences and insightfulness. In line with the observed decreases in oscillations at 1.5-20 Hz, it has previously been reported that the serotonergic hallucinogenic brew ayahuasca attenuated ongoing oscillations up to 20 Hz, with similar maximum effects in the Fig.Statistical maps of the voxel-wise effect of psilocybin on neuronal oscillations at 1.5-4 Hz (delta; top row), 4-8 Hz (theta; second row), 8-10.5 Hz (alpha1; third row), 10.5-13 Hz (alpha2; fourth row), 13-20 Hz (beta1; fifth row), 20-30 Hz (beta2; sixth row), 30-45 Hz (gamma1; seventh row), and 55-100 Hz (gamma2; bottom row) in the eyes-closed condition. Blue depicts voxels where neuronal oscillations were significantly decreased by psilocybin (p <0.05, corrected). Yellow depicts voxels where neuronal oscillations were significantly increased by psilocybin (p<0.05, corrected) (color figure online) theta/alpha frequency range). Both psilocybin and the main psychoactive compound of ayahuasca, DMT, are thought to induce their psychological effect predominantly by activation of 5-HT2A receptors, and activation of these receptors mediated the psilocybin-induced decrease in ongoing alpha oscillations). Thus, our findings add to the evidence that a decrease of ongoing oscillations below 20 Hz, particularly theta/alpha oscillations, may be a common mechanism of action of serotonergic hallucinogens such as psilocybin and DMT. Using source localization, we further revealed that this psilocybin-induced decrease in lower-frequency oscillations was localized within an extended network that included the PCC, the RSC, the ACC, and parahippocampal regions. Interestingly, this network strongly overlaps with the defaultmode network (DMN), which has been shown to be modulated by psilocybin in PET and fMRI studies. Activity within the DMN has been associated with lower-frequency oscillations) and with altered states of consciousness induced for instance by anesthetics, serotonergic hallucinogens, and meditation). Thus, our findings indicate that psilocybin modulates default-mode functions by decreasing ongoing lowerfrequency oscillations within this network, which may contribute to the psilocybin-induced alterations in the state of consciousness. Specifically, lower frequency oscillations, particularly in the alpha range, mediate rhythmic cortical inhibition of neuronal ensembles. Thus, the strong decrease in lower-frequency oscillations seen in this study may be indicative of a psilocybin-induced shift of the resting excitation/inhibition balance (E/I balance) toward excitation. This interpretation is also supported by the slight psilocybininduced increase in high-gamma oscillations because gamma oscillations have been strongly associated with neuronal excitation. Given the crucial role of lowerfrequency oscillations in structuring processes at the cellular level), the systemic level, and in consciousness, any profound decrease in lower-frequency oscillations is likely to disrupt the ordinary temporal structure of neuronal processes. Taken together, these findings suggest that psilocybin elevates the E/I balance and disrupts the temporal structure of neuronal processes by decreasing lower-frequency (<20 Hz) oscillations within the extended DMN. This network has been implicated in self-referential processing; therefore, the increased excitability and disrupted temporal structure of neuronal processes may alter self-referential processes and thereby lead to psilocybin-induced alterations in a state of consciousness such as an increased sense of unity with the environment. However, although these alterations may play a role in altering consciousness, correlation analysis indicated that these alterations are not sufficient to alter consciousness because only the correlation between psilocybininduced insightfulness and alpha2 (10.5-13 Hz) oscillations in the posterior occipito-parietal region during the eyes-open condition was significant after correction for multiple comparisons. In contrast to the weak associations between current source density and state of consciousness, lagged phase synchronization was strongly associated with the psilocybin-induced state of consciousness. Given the crucial role of phasesynchronization in coordinating activity across brain areas, this finding supports the view that neural integration, rather than activity, underlies the state of consciousness. Specifically, we found that the intensity of psilocybininduced insightfulness was associated with lagged phase synchronization of delta oscillations between parahippocampal regions, between parahippocampal regions and the RSC as well as between parahippocampal regions and the lateral orbitofrontal cortex. Because phase synchronization of parahippocampal oscillations in this frequency range has previously been linked to autobiographical memory retrieval) and to the attribution of valence in memory, our finding suggests that psilocybin-induced insightfulness may be associated with increased retrieval and reattribution of autobiographic memories. In addition, scores of the spiritual experiences subscale of the 5D-ASC questionnaire were associated with increased lagged phase synchronization of delta oscillations between parahippocampal regions and the RSC. The RSC has previously been implicated in coding the location of oneself within a global spatial context, and therefore, our finding may suggest that with increasing intensity of spiritual experiences, the self is reorganized within the global spatial context through phase synchronization of delta oscillations. These interpretations fit well with the phenomenological descriptions of hallucinogen-induced insightfulness and spiritual experiences. Hallucinogen-induced insightfulness is characterized by a deep understanding of personal life and existence, which could well explain, why increased autobiographical retrieval and reattribution processes may be present during insightfulness. Furthermore, hallucinogen-induced spiritual experiences include a shift in the perception of one's self and one's existenceand were defined in our study according to the 5D- ASC questionnaire as a profound experience of awe and connectedness to a superior power. These phenomenological descriptions match well with our interpretation that psilocybin-induced spiritual experiences are associated by a reorganization of the self within the global spatial context mediated by phase synchronization of delta oscillations. Finally, phenomenological studies found that psilocybin-induced insightfulness and spiritual experience often occur together, which fits well with our finding that these states are mediated by phasesynchronization in a partially overlapping network. Interestingly, the revealed network phase-synchronization processes were specifically associated with insightfulness and spiritual experiences, as defined by the 5D-ASC questionnaire, but not with other psilocybin-induced phenomena such as blissful states or disembodiment. Furthermore, after correction for multiple comparison, the correlation was only seen during eyes-closed condition. These findings suggest first that the revealed associations are specific for these two experiences, but likely additional network processes are implicated in a full blown mystical/spiritual experience that fulfills all the criteria byand is quantified by the SOCQ questionnaires. Second, our results suggest that eyes-closed conditions might be particularly suitable to investigate the neuronal processes associated with insightfulness and spiritual experiences, which is in accordance with the use of eye-shades in some previous phenomenological studies that aimed to specifically investigate psilocybin-induced spiritual experiences. The neuronal network processes we identified as underlying spiritual experiences and insightfulness may constitute a crucial pathway that can be modulated by serotonergic receptors to regulate mental health. This notion is supported by reports that spiritual experiences promoted sustained well-being and resilienceand that psilocybin had therapeutic effects in treating mood disordersand in reducing anxiety in terminal cancer patients). Thus, in future studies, it will be interesting to test whether lagged phase synchronization between the RSC, the parahippocampus, and the lateral orbitofrontal area can promote mental health through the activation and reattribution of autobiographical memory and the reallocation of the self in a global spatiotemporal context.
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