This fMRI study (2020) improves our understanding of how LSD changes brain function over time and how subjective effects (e.g. ego dissolution) map onto these changes.
Investigating changes in brain function induced by mind-altering substances such as LSD is a powerful method for interrogating and understanding how mind interfaces with brain, by connecting novel psychological phenomena with their neurobiological correlates. LSD is known to increase measures of brain complexity, potentially reflecting a neurobiological correlate of the especially rich phenomenological content of psychedelic-induced experiences. Yet although the subjective stream of consciousness is a constant ebb and flow, no studies to date have investigated how LSD influences the dynamics of functional connectivity in the human brain. Focusing on the two fundamental network properties of integration and segregation, here we combined graph theory and dynamic functional connectivity from resting-state functional MRI to examine time-resolved effects of LSD on brain networks properties and subjective experiences. Our main finding is that the effects of LSD on brain function and subjective experience are non-uniform in time: LSD makes globally segregated sub-states of dynamic functional connectivity more complex, and weakens the relationship between functional and anatomical connectivity. On a regional level, LSD reduces functional connectivity of the anterior medial prefrontal cortex, specifically during states of high segregation. Time-specific effects were correlated with different aspects of subjective experiences; in particular, ego dissolution was predicted by increased small-world organisation during a state of high global integration. These results reveal a more nuanced, temporally-specific picture of altered brain connectivity and complexity under psychedelics than has previously been reported.
Papers cited by this study that are also in Blossom
Atasoy, S., Leor, R., Kaelen, M. et al. · Scientific Reports (2017)
Atasoy, S., Vohryzek, J., Deco, G. et al. · Progress in Brain Research (2018)
Carhart-Harris, R. L. · Neuropharmacology (2018)
Carhart-Harris, R. L., Erritzoe, D., Williams, T. et al. · PNAS (2012)
Luppi and colleagues situate their study within recent efforts to link psychedelic-induced alterations of consciousness to their neurobiological substrates using non-invasive imaging. Prior work indicates that serotonergic psychedelics such as LSD, psilocybin and DMT increase measures of brain complexity and alter functional connectivity, typically reducing within-network integrity while increasing between-network coupling. The authors note that the stream of consciousness is inherently dynamic, and that previous studies have largely neglected temporal fluctuations in functional connectivity. They argue that integration and segregation are fundamental network properties relevant to consciousness and hypothesise that LSD's effects may be temporally specific rather than uniform across time. This study therefore aimed to combine graph theory with dynamic functional connectivity (dFC) from resting-state fMRI to test whether LSD alters time-resolved network organisation, focusing on integrated versus segregated dynamic sub-states. Following the Entropic/Anarchic Brain framework, the researchers predicted that LSD would produce effects broadly opposite to those observed during loss of consciousness, and that these effects would be differentially expressed during integrated and segregated dFC sub-states. The investigation used a placebo-controlled design in healthy volunteers with prior psychedelic experience to examine network-level and regional changes and their relation to subjective experience.
Fifteen healthy volunteers (final N = 15 after one aborted experiment and four exclusions for excessive motion) underwent two imaging sessions 14 days apart in a placebo-controlled within-subject design. On one day participants received placebo (10 mL saline) and on the other 75 μg LSD in 10 mL saline, infused over 2 minutes and administered 115 minutes before fMRI scanning. Imaging comprised three seven-minute resting-state BOLD scans with eyes closed; analyses reported here used the first and third (no-music) scans, each 7:20 minutes long. Subjective ratings were obtained in-scanner using VAS and post-scan using the 11-item Altered States of Consciousness (ASC) scale. Preprocessing used the CONN toolbox and SPM12 routines: removal of the first three volumes, realignment, slice-timing correction, outlier detection (art), normalisation to MNI space (2 mm), and 6 mm FWHM smoothing. Denoising employed anatomical CompCor (aCompCor) to regress out five white-matter and five CSF principal components, six motion parameters plus derivatives, scrubbing of outlier volumes, session effects, linear detrending and band-pass filtering (0.008–0.09 Hz). Global signal regression was deliberately avoided. Excess motion was defined as >15% of volumes with mean framewise displacement >0.5; mean framewise displacement was included as a covariate because it was higher under LSD (Placebo mean = 0.079, SD = 0.026; LSD mean = 0.129, SD = 0.039; t(14) = -6.34, p < 0.001). Functional parcellation used an augmented Schaefer-232 atlas (200 cortical + 32 subcortical ROIs); robustness checks employed a finer Schaefer-454 (400 + 54) and the Brainnetome-246 (210 + 36). Region-wise BOLD timecourses were averaged and pairwise Pearson correlations computed to form FC matrices for each full scan. Dynamic functional connectivity was estimated using tapered sliding windows obtained by convolving a 22-TR (44s) rectangular window with a 3-TR Gaussian, sliding in 1-TR steps; this yielded a sequence of 232×232 FC matrices per timepoint. Dynamic sub-states were identified via the cartographic profile: within each window, nodes' participation coefficient and within-module degree Z-score were computed from graph-theoretical module assignments. A k-means clustering (k = 2, supported by silhouette analysis) of the joint histogram of these measures assigned windows to predominantly integrated or predominantly segregated sub-states. For each subject and sub-state, centroid FC matrices (median of assigned windows), the proportion of time spent in each sub-state, and the entropy of the sub-state sequence were computed. Stationarity of dynamics was assessed by comparing empirical results to surrogate data generated with pairwise 2-D VAR(4) models. Network-level measures included the prevalence of anticorrelations (proportion of negative edges), similarity between functional and structural connectivity (Spearman correlation and Hamming distance versus a group-average structural connectome from 1,021 HCP subjects), small-world propensity (ϕ, bounded 0–1, computed both on thresholded binary networks at densities 10%–25% and on weighted non-negative networks), and a measure of functional complexity based on the distribution of pairwise correlations. Statistical testing used two-tailed robust linear models with mean framewise displacement as covariate; correlations with subjective measures used Spearman's ρ and were interpreted only when reproducible across all three parcellations. Network-based Statistic (NBS) was applied to identify connected components of edges differing under LSD, with an intensity F-threshold of 10 (robustness checks at F = 12 and an extent-based threshold of 10).
Sample and validation. After exclusions, 15 participants were analysed. The cartographic profile reliably separated two dynamic sub-states (k = 2 selected by silhouette). The proportion of time spent in the predominantly integrated sub-state was approximately 0.69 (SD = 0.07) in placebo and was preserved under LSD, indicating no change in gross temporal allocation between integrated and segregated sub-states. Empirical proportions were greater than stationary VAR surrogates for both placebo (empirical M = 0.69 vs surrogate M = 0.51, t(14) = 2.42, p = 0.030) and LSD (empirical M = 0.69 vs surrogate M = 0.55, t(14) = 2.91, p = 0.014), supporting genuine dynamical structure. Entropy of sub-state alternation did not change significantly between conditions. Time-averaged and sub-state-specific FC. Time-averaged FC showed a predominance of global FC increases under LSD along with disconnections between prefrontal and posterior/temporal regions. Dynamic, sub-state-specific analyses revealed that the predominantly integrated sub-state exhibited no significant LSD-induced FC alterations, whereas the predominantly segregated sub-state displayed both increases and decreases in FC. Notably, the anterior medial prefrontal cortex (mPFC) showed reduced FC specifically during the segregated sub-state; time-averaged FC instead showed stronger reductions in medial orbitofrontal cortex. The segregated sub-state had net increases in somatomotor and auditory cortex connectivity and net decreases in key default mode network nodes (medial PFC, bilateral angular gyri, temporal poles). The posterior cingulate reduced connectivity with visual regions but increased connectivity with executive-control regions, and the thalamus increased connectivity with orbitofrontal, temporal cortices and bilateral amygdalae. These NBS findings were robust across parcellations, with the exception that time-averaged FC differences were not significant with the Brainnetome atlas though the segregated sub-state pattern remained. Structural-functional similarity and anticorrelations. There was no significant change in similarity between time-averaged FC and the structural connectome. However, during the predominantly segregated sub-state, LSD reduced the similarity of FC to structural connectivity (lower Spearman correlation and increased Hamming distance), indicating greater decoupling from anatomy; no significant effect was observed in the integrated sub-state. Regarding anticorrelations, LSD reduced the overall proportion of negative edges across the full scan, but dynamic analysis showed that this reduction was specific to the segregated sub-state; the integrated sub-state did not show significant LSD-related suppression of anticorrelations. Small-world propensity and functional complexity. Small-world propensity (ϕ) increased under LSD. For thresholded binary networks the increase was evident during the segregated sub-state and for time-averaged FC; when weighted networks including weaker (non-negative) edges were analysed, increased ϕ was detected for both integrated and segregated sub-states. The net rise in small-world propensity arose from opposing trends: ΔL (deviation of path length from random) increased under LSD (which would lower ϕ), while ΔC (deviation of clustering from lattice) decreased (which increased ϕ), with the latter effect predominating. Functional complexity (a measure derived from the distribution of pairwise correlations) increased under LSD overall, but this effect was confined to the segregated sub-state and was not observed in the integrated sub-state. Robustness and correlations with subjective experience. Key results were robust across alternative parcellations with some exceptions noted for specific metrics. Exploratory correlations reproducible across all three parcellations included: in the predominantly integrated sub-state, increases in weighted small-world propensity correlated positively with ASC blissful state (Spearman's ρ = 0.65, p = 0.009), ASC complex imagery (ρ = 0.68, p = 0.006) and VAS ego dissolution (ρ = 0.57, p = 0.027). In the predominantly segregated sub-state, changes in the prevalence of anticorrelations correlated with ASC disembodiment (ρ = 0.62, p = 0.013) and ASC elementary imagery (ρ = 0.61, p = 0.015). None of the reported brain measures correlated significantly with mean framewise displacement for the Schaefer parcellations, supporting that motion was not driving these effects.
Luppi and colleagues interpret their results as showing that LSD's effects on brain function and subjective experience are temporally specific rather than uniform. Although LSD did not change the overall fraction of time the brain spent in predominantly integrated versus segregated sub-states, it differentially altered network properties within those sub-states. The apparent paradox that both LSD and loss of consciousness reduce anticorrelations is resolved by this temporal decomposition: reduced anticorrelations in anaesthesia are most pronounced during integrated sub-states, whereas LSD suppresses anticorrelations primarily during segregated sub-states. This sub-state specificity also extended to structural-functional coupling and complexity: LSD increased functional complexity and reduced similarity to the structural connectome, but these effects were concentrated in segregated moments when functional patterns are already less constrained by anatomy. The authors situate these findings within the REBUS/Anarchic Brain framework, proposing that LSD weakens the influence of anatomical priors on functional coupling, allowing exploration of a broader repertoire of connectivity patterns. A specific regional finding—the reduced functional connectivity of anterior mPFC during segregated sub-states—is linked to possible attenuation of reality-monitoring processes; the authors note parallels between mPFC disconnection in LSD and observations in schizophrenia, and propose that transient reductions in top-down constraint may underlie hallmark psychedelic phenomena. Small-world propensity increased under LSD, reflecting an increased local clustering compensated by longer path lengths; importantly, increases in integrated-state small-world propensity predicted subjective reports of bliss, complex imagery and ego dissolution. The authors highlight that ego-dissolution correlations were temporally specific and may be relevant for therapeutic mechanisms. Several limitations are acknowledged. The dataset is relatively small and previously studied, so replication in independent and larger samples is necessary. Blinding is imperfect because LSD's effects are overt; an active placebo could address expectancy and arousal confounds. Head motion differed between conditions, and although aCompCor denoising, participant exclusion criteria and inclusion of mean framewise displacement as a covariate were employed, residual confounding cannot be fully excluded. Structural connectivity was taken from a group-average template rather than individual diffusion data, so structural-functional deviations are relative to the population average. Methodological differences between approaches to brain dynamics (e.g. sliding-window cartographic profile versus LEiDA or connectome-harmonic decomposition) mean that direct mapping between findings across methods is non-trivial, although converging evidence from different techniques was noted. Finally, the authors call for higher temporal resolution modalities (EEG/MEG) and improved experience sampling to better link dynamic brain states with subjective experience.
The primary novel conclusion is that LSD's effects on brain function and subjective experience depend on the brain's dynamic state at a given time. Specifically, LSD makes globally segregated sub-states more complex and more decoupled from anatomical constraints, and reduces functional connectivity of anterior medial prefrontal cortex during those segregated moments. These temporally specific alterations align with the REBUS framework, suggesting that LSD weakens anatomical priors on functional connectivity and thereby facilitates exploration of diverse connectivity patterns. Additionally, increased small-world propensity during predominantly integrated sub-states predicted ego dissolution, indicating that different dynamic sub-states relate to distinct subjective features of the psychedelic experience.
Due to its potent temporary effects on both the human mind and brain, the serotonergic psychedelic LSD represents a powerful method for connecting psychological phenomena to their neurobiological correlates, and improving our understanding of both. However, by definition, the stream of consciousness is dynamic and always flowing: ignoring this temporal aspect may neglect a key aspect of consciousness and its psychedelic-induced alterations. Focusing on two fundamental properties of both the human mind and brain -integration and segregationhere we combined fMRI dynamic functional connectivity and graph theory to investigate how the classic serotonergic psychedelic LSD modifies brain function and its dynamics under task-free, eyes-closed resting-state conditions, by investigating the network characteristics in a temporally sensitive way. Highlighting the crucial importance of considering brain dynamics when investigating states of altered consciousness, our first observation was that the consciousness-altering effects of LSD show prominent temporal aspects. In particular, these effects do not influence the overall allocation of time between predominantly integrated and segregated sub-states -echoing the results obtained in both anaesthesia and disorders of consciousness. Rather, LSD differentially affects the network properties of predominantly integrated and segregated sub-states. A robustly observed neural marker of the psychedelic experience induced by various drugs is the suppression of anticorrelations between brain regions. Reduced anticorrelations are also reliably observed during loss of consciousness induced by anaesthesia or brain injury; however, our findings resolve this apparent paradox. Recent evidence indicates that reduced anticorrelations in anaesthesia and disorders of consciousness are most prominent during the integrated sub-state, whereas the present results reveal that LSD suppresses anticorrelations during the predominantly segregated sub-state. Indeed, the correlation of this effect with subjective experiences of disembodiment and elementary imagery was selective for the segregated sub-state. Thus, by considering brain network dynamics we can discover that apparently similar effects of LSD and loss of consciousness (i.e. reduced anticorrelations in time-averaged FC) actually have their origins in different dynamic sub-states -thereby reconciling apparently opposite observations, and demonstrating the value of taking a dynamic approach to the study of altered brain function. It has been postulated that the functional complexity of the resting human brain operates near the maximum supported by the underlying structural connectome. Here, we show that the state of altered consciousness induced by LSD corresponds to an additional, abnormal increase in functional complexity of the brain as a result of LSD. Remarkably, this effect is not uniform in time, but rather, it is only observed during moments when the brain is characterised by a predominantly segregated pattern of functional connectivity -coinciding with reduced similarity between functional connectivity and the underlying pattern of structural connections (which is the oppo- site of what is typically found during anaesthesia). Further highlighting the importance of considering network dynamics, this structuralfunctional decoupling is exclusively observed during the predominantly segregated sub-state (i.e. this effect is not apparent when only considering time-averaged FC). At baseline (placebo condition), the predominantly segregated sub-state is already more decoupled from structural connectivity than the integrated sub-state (in line with the results of), and also exhibits larger functional complexity. Thus, LSD appears to induce especially complex patterns of functional connectivity by inducing additional decoupling of FC from the underlying structural connectome, precisely during those times when structural-functional coupling is already at its lowest. This evidence is also consistent with previous results obtained by Atasoy and colleagues in the same LSD dataset, as well as in psilocybin, by using an alternative method to study brain dynamics, known as connectome harmonic decompositions (CHD). This technique decomposes brain activity into a set of progressively more fine-grained patterns derived from the human connectome (termed "connectome harmonics ");observed that LSD and psilocybin induce a reduction in the contribution of coarse-grained harmonics -which according to recent evidence are precisely the harmonics most strongly coupled to the underlying structural connectome. Thus, two different ways of investigating brain dynamics converge to reveal a psychedelic-induced decoupling of function from structure. Reduced similarity between structural and functional connectivity indicates that under the effects of LSD, brain regions interact functionally in a way that is less constrained than usual by the presence or absence of an underlying anatomical connection. Anatomical brain connectivity may be understood as representing the organism's expectation about which brain regions should be exchanging information with each other, sculpted by the combined effects of evolution and experience, in accordance with Donald Hebb's famous dictum that "neurons that fire together, wire together ". In other words, anatomical connectivity may be seen as representing a prior (in Bayesian terms) on functional connectivity. When considered in this way, the increased correlation between structural and functional connectivity during anaesthetic-induced unconsciousnesswould reflect the fact that incoming external information is being processed only to a minimal degreeand therefore the patterns of functional connectivity are primarily dictated by structurally-encoded priors. In contrast, the reduced structural-functional correlation that we observed during the psychedelic state induced by LSD would be consistent with a reduced effect of priors on cognition, as postulated by the REBUS frame-work. Being less constrained by preexisting priors due to the effects of LSD, the brain is free to explore a variety of functional connectivity patterns that go beyond those dictated by anatomy -presumably resulting in the unusual beliefs and experiences reported during the psychedelic state, and reflected by increased functional complexity. Importantly, this observation is only possible thanks to our decomposition of functional connectivity into predominantly integrated and segregated dynamic sub-states. The large-scale reorganisation of functional connectivity during the segregated sub-state crucially includes LSD-induced disconnections between posterior and frontal regions -especially the left anterior medial prefrontal cortex. This is particularly intriguing because anterior mPFC has been consistently and specifically implicated in the cognitive process known as reality monitoring, which is the ability to correctly discriminate whether information is derived exogenously (from perceptual processes) or generated endogenously (from thoughts and imagination). Dysfunction of this process is thought to underlie the auditory and visual hallucinations that are a prevalent feature of schizophrenia. Anterior mPFC is consistently found to be both hypoactive during tasks involving reality monitoring in patients with schizophrenia, who experience auditory and visual hallucinations. Intriguingly, in schizophrenic patients, the same region also exhibits disconnections with posterior regions, akin to what was observed in the present study as a result of LSD administration. Remarkably, just like the aforementioned reduction in structural-functional coupling, mPFC disconnection was also exclusively observed in the predominantly segregated sub-state, and not when considering time-averaged FC (which instead exhibited disconnections from a more ventral portion of PFC). Thus, we speculate that the anterior mPFC disconnections induced by LSD during the predominantly segregated state, may correspond to attenuated engagement of top-down reality monitoring processes. This is again in accordance with what the REBUS/Anarchic Brain hypothesis of psychedelic action ( Carhart-Harris and Friston, 2019 ) postulates, corresponding to a "suspension of disbelief " right at the moment when the most diverse patterns of connectivity are being explored, and when the functional connectome is minimally constrained by the hardwired connections between brain regions. This hypothesis may be empirically tested in future work, directly assessing reality monitoring processing during the psychedelic state, for instance by means of experience sampling approache. More broadly, these observations are also consistent with the main tenet shared by theories of psychedelic action from the 19 th , 20 th and 21 st century: spanning from the entropic brain hypothesis and predictive processing framework (the two main pillars of the REBUS/Anarchic brain hypothesis) but also including psychoanalytic and filtration accounts: namely, that psychedelics "perturb adaptive mechanisms which normally constrain perception, emotion, cognition, and self-reference ", page 16). Finally, both the predominantly integrated and segregated sub-states exhibited increased small-world propensity -the opposite of what is observed with loss of consciousness. Unlike the other results reported here, the LSD-induced increased in small-world propensity was observed in both integrated and segregated dynamic sub-states (although thresholding the network to only keep the strongest connections changed this behaviour, highlighting the important role of weak edges in the small-world topology of brain networks). Small-worldness reflects optimal balance of local and global processing in a network, by combining high local clustering (facilitation sharing of information at a local level) with a short characteristic path length that dramatically reduces the cost of global information transmission. Crucially, the overall increase in small-world propensity observed here arose from the balance of two opposing trends: namely, the deviation of characteristic path length from a corresponding random network ( Δ L ) increased under LSD, reducing the network's small-world propensity; however, this effect was more than compensated by a reduction in the deviation of the network's clustering coefficient from that of a regular network ( Δ C ) -resulting in overall increased small-world propensity. In other words, under the effects of LSD the brain appears to shift the balance of information processing towards a more localised pattern. These findings are in line with evidence obtained in time-averaged networks after ingestion of ayahuasca, showing increased clustering coefficient but decreased characteristic path length. However, small-world propensity also exhibited time-specific effects that could not be observed from just considering time-averaged FC: namely, only the increase pertaining to the predominantly integrated state was consistently predictive of subjective experiences induced by LSD: blissful feeling, complex imagery, and ego dissolution. The discovery that LSD-induced ego-dissolution exhibits temporally-specific effects merits special attention because the extent of ego-dissolution experienced during the psychedelic experience has been repeatedly found to predict positive clinical outcomes following psychedelic administration. Thus, advancing our understanding of the dynamic effects of psychedelics on brain function, and the interaction between brain integration and ego dissolution in particular, may hold further promise for our understanding of the therapeutic effects of psychedelics. Our results suggest that the predominantly integrated sub-state may be especially relevant for supporting the feeling of integrity of one's sense of self, as indicated by the positive correlation between perturbed balance of local-global processing (quantified by small-world propensity) and subjective feeling of ego dissolution. Indeed, it stands to reason that states of relatively high brain integration should be especially relevant for one's sense of self, when considering the intrinsically integrative nature of the self, which brings together distinct sensory streams into a unified "stream of consciousness " as well as the continuity between past and present.
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