Connectome-harmonic decomposition of human brain activity reveals dynamical repertoire re-organization under LSD

Selen Atasoy, Leor Roseman, Mendel Kaelen, Morten L. Kringelbach, Gustavo Deco & Robin L. Carhart-Harris

Scientific Reports | 7: 17661 |

DOI:10.1038/s41598-017-17546-0

www.nature.com/scientificreports

Recent studies have started to elucidate the effects of lysergic acid diethylamide (LSD) on the human brain but the underlying dynamics are not yet fully understood. Here we used ’connectome-harmonic decomposition’, a novel method to investigate the dynamical changes in brain states. We found that LSD alters the energy and the power of individual harmonic brain states in a frequency-selective manner. Remarkably, this leads to an expansion of the repertoire of active brain states, suggestive of a general re-organization of brain dynamics given the non-random increase in co-activation across frequencies. Interestingly, the frequency distribution of the active repertoire of brain states under LSD closely follows power-laws indicating a re-organization of the dynamics at the edge of criticality. Beyond the present findings, these methods open up for a better understanding of the complex brain dynamics in health and disease.

The psychoactive effects of lysergic acid diethylamide (LSD) were discovered in 1943 and began to be fully reported on in the late 1940s1 and early 1950s2. For a period of approximately 15 years, LSD and related psychedelics were used as tools to explore and understand consciousness3, psychopathology4 and also to treat mental illness5. In addition to the LSD’s recognised effects on perception, it was reported to ‘loosen’ constraints on consciousness, expanding its breadth, without compromising wakefulness. Indeed, it was said of LSD and related psychedelics, that they could serve as ‘microscopes’ or ‘telescopes’ for psychology, allowing scientists to see more of the mind than is normally visible6. For various reasons7, psychology has been slow to embrace and exploit this powerful scientific tool, but now, with significant advances in modern functional neuroimaging and underperformance in medical psychiatry8, there are significant incentives to do so.

Previous functional magnetic resonance imaging (fMRI) and magnetoencephalography (MEG) work has reported increased visual cortex blood flow, increased whole-brain functional integration (decreased modulatory organization), and decreased oscillatory power across a broad frequency range under LSD9,10.

These findings are based on conventional neuroimage analysis methods and although they offer a useful impression of the neural correlates of the LSD state, they provide limited information on whole-brain dynamics. Recent research has begun to postulate changes in brain dynamics that may account for the putative broadening of consciousness under psychedelics11; however, experimental evidence for the hypothesized dynamical changes is limited12.

A fundamental limitation to understanding the nature of these spatio-temporal changes, is the lack of mathematical tools and methods particularly tailored to grasp the complex dynamics of cortical activity13,14. Here we describe a novel method to decompose resting-state fMRI data under LSD and placebo into a set of independent, frequency-specific brain states.

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