Psilocybin enhances insightfulness in meditation: a perspective on the global topology of brain imaging during meditation - PubMed (original) (raw)

Psilocybin enhances insightfulness in meditation: a perspective on the global topology of brain imaging during meditation

Berit Singer et al. Sci Rep. 2024.

Erratum in

Abstract

In this study, for the first time, we explored a dataset of functional magnetic resonance images collected during focused attention and open monitoring meditation before and after a five-day psilocybin-assisted meditation retreat using a recently established approach, based on the Mapper algorithm from topological data analysis. After generating subject-specific maps for two groups (psilocybin vs. placebo, 18 subjects/group) of experienced meditators, organizational principles were uncovered using graph topological tools, including the optimal transport (OT) distance, a geometrically rich measure of similarity between brain activity patterns. This revealed characteristics of the topology (i.e. shape) in space (i.e. abstract space of voxels) and time dimension of whole-brain activity patterns during different styles of meditation and psilocybin-induced alterations. Most interestingly, we found that (psilocybin-induced) positive derealization, which fosters insightfulness specifically when accompanied by enhanced open-monitoring meditation, was linked to the OT distance between open-monitoring and resting state. Our findings suggest that enhanced meta-awareness through meditation practice in experienced meditators combined with potential psilocybin-induced positive alterations in perception mediate insightfulness. Together, these findings provide a novel perspective on meditation and psychedelics that may reveal potential novel brain markers for positive synergistic effects between mindfulness practices and psilocybin.

© 2024. The Author(s).

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Conflict of interest statement

The authors declare no competing interests.

Figures

Figure 1

Figure 1

(a) A representative Mapper shape graph of one subject (5119) produced with the visualization library

DyNeuSR

. Each color represents the distribution of an MS (Table 1) in the subject-specific landscape of brain states. (b) The network is a schematic picture of the average topological organization of Mapper shape graphs that are shared across all subjects. The nodes are labeled according to the six meditation states (MS), (Table 1). For example, we found that the closeness centrality of the OM significantly increased postretreat, which is represented by the central position of the OM post-node. The length of the edges represents the average OT distance (over all subjects) between the MSs. For example, the OT distance between FA2 and OM2 is smaller than the OT distance between FA1 and OM1. Finally, the diameter of the node represents the diameter of the corresponding MS. Significant increases in the measurements due to retreat and drug effects are annotated by blue and red stars, respectively. Similarly, decreases are annotated by blue and red accidentals, respectively. The star in the bracket near node FA2 indicates that the effect is most likely neglectable. Two stars near OM2 indicate that two measurements (diameter and centrality) were significant. Black accidentals indicate a significant decrease in the distance for the group with low positive derealization. The detailed statistical descriptions are given below. (c) Pearson correlations of all graph measures with p values according to the color bar (corrected for 21*21 multiple comparisons). This Figure illustrates how the OT distances are strongly colinear (for topological reasons).

Figure 2

Figure 2

(a) A heatmap representing the statistical tests; colored boxes indicate significant differences according to the p values annotated and according to the color bar (multiple comparison correction of the first six rows by ∗3, see Methods). For notationsin the rows, see Table 1. The first three columns represent the ANOVA tests with drug (psilocybin vs. placebo), retreat (pre vs. post), and interaction effects of drug*retreat, respectively. The fourth column represents the paired t tests comparing pre- vs. postretreat deata over the whole dataset. The fifth column represents the colorred results of the independent t tests of psilocybin vs. placebo postretreat. (b) Distributions of the graph measures plotted according to the significance tests in 2a. Notations; ns: not significant or p>0.05, ∗:1.00e-02<p<=5.00e-02, ∗∗:1.00e-03<p<=1.00e-02, and ∗∗∗:1.00e-04<p<=1.00e-03. (c) Independent t tests for the drug effect on the OT distances before vs. after the retreat of the same meditation styles. (d) Significant (according to the t test in (c)) differences (placebo vs. psilocybin) in the distributions of the distances between OM1 and OM2 and between RS1 and RS2. The notations are the same as before.

Figure 3

Figure 3

Kendal rank correlations and p values (according to the color bar, up to a p value of 0.1) of topological descriptors with rankings from the altered states of consciousness (ASC) questionaire, corrected for effective number of multiple comparison (*10, see Methods). Significant (p<0.05) correlations are marked by a ∗. The three distances (d(_OM_1, _OM_2), d(_RS_1, _RS_2) and d(_OM_2, _RS_2)) are strongly correlated (see Fig. 1c) and show significant drug effects (see Fig. 2).

Figure 4

Figure 4

(a) Correlation between d(_OM_2, _RS_2) and positive derealization. The skewness in the data was noticeable, and the placebo group tended to accumulate toward one end of the plot. Notably, the results of the mixed linear model are stronger since they show a retreat effect and a combined effect of retreat and positive derealization. (b) Correlation between d(_OM_2, _RS_2) and positive derealization for the psilocybin group. (c) Significant decrease in d(OM∗,RS∗) due to retreat for those subjects with positive derealization ratings below the median. (d) Visualisation of the linear model for the dependent variable insightfulness with two explanatory variables (for the whole group). Positive derealization and d(_OM_1, _OM_2) together provide better predictions of insightfulness than does positive derealization alone. The data were split into two equal groups at their median value (indicated by the two colors and the values are in brackets on the right). (e) Same as 4c but for the psilocybin group.

Figure 5

Figure 5

A hypothetical topological model of core phenomenological features and their relationships with mindfulness-related practices. Here, the distance between the nodes represents the topologically measured OT distance in the landscape of meditative states (i.e. Mapper shape graph of FA, OM and RS) and reveals relationships and interactions (overlap and similarity) of mindfulness-related practices at the level of brain activity. This perspective may provide insights into how changes in consciousness and perception during meditation or psilocybin-assisted mindfulness practices translate into alterations in the topological landscape and allow further exploration into the sometimes complementary and opposing yet potentially synergistic effects between mindfulness-related practices and the phenomenology of psychedelic experiences. Hypothetically, certain changes in perception, cognition and consciousness are associated with increased OT distances between FA, OM, or RS (i.e., less interaction, overlap, or similarity), which are represented by arrows pointing away from the center. Conversely, other changes in perception, cognition and consciousness may be associated with decreased OT distance between FA, OM, or RS (i.e., more interaction, overlap, or similarity), which are represented by arrows pointing toward the center. This theory is consistent with our findings (Figs. 2 and 3). Decreased d(FA∗,OM∗) might be an indicator of increased meta-awareness while monitoring attention and distraction. Indeed, we observed that d(FA, OM) decreased due to the retreat. Similarly, a decreased d(RS∗,OM∗) might be an indicator of meta-awareness of mind wandering or informational content, which is supported by the observation that d(RS∗,OM∗) significantly decreased due to the retreat in participants with lower ratings of positive derealization (Fig. 4c). The correlation of d(RS∗,OM∗) with positive derealization supports the idea that increased informational content increases the OT distance between RS and OM. While increased effortlessness of focus presumably decreases d(FA∗,RS∗), decreased distraction increases d(FA∗,RS∗)). Notably, this could be a plausible explanation for our observation that d(FA∗,RS∗) did not change pre- or postretreat since the two effects cancel each other out.

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