LSD-induced increase of Ising temperature and algorithmic complexity of brain dynamics

• Published in: PLoS computational biology Vol. 19; no. 2; p. e1010811
• Main Authors: Ruffini, Giulio, Damiani, Giada, Lozano-Soldevilla, Diego, Deco, Nikolas, Rosas, Fernando E, Kiani, Narsis A, Ponce-Alvarez, Adrián, Kringelbach, Morten L, Carhart-Harris, Robin, Deco, Gustavo
• Format: Journal Article
• Language: English
• Published: United States Public Library of Science 03.02.2023; Public Library of Science (PLoS)
• Subjects: Algorithms; Biology and Life Sciences; Brain; Brain architecture; Brain mapping; Brain research; Cerebral hemispheres; Complexity; Computational neuroscience; Computer and Information Sciences; Consciousness; Critical point; Dictionaries; Drug dosages; Dynamics; Entropy; Experimental data; Formalism; Functional magnetic resonance imaging; Hallucinogens - pharmacology; Health aspects; Humans; Ingestion; Ising model; LSD; LSD (Drug); Lysergic acid diethylamide; Lysergic Acid Diethylamide - pharmacology; Lysergide; Magnetic resonance imaging; Magnetic Resonance Imaging - methods; Maximum entropy; Medicin och hälsovetenskap; Medicine and Health Sciences; Nervous system; Neural networks; Neuroimaging; Phase transitions; Physical Sciences; Placebos; Psychedelic drugs; Repertoire; Research and Analysis Methods; Statistical physics; Temperature; Thermal properties; Time series; Spain
• ISSN: 1553-7358; 1553-734X; 1553-7358
• DOI: 10.1371/journal.pcbi.1010811

A topic of growing interest in computational neuroscience is the discovery of fundamental principles underlying global dynamics and the self-organization of the brain. In particular, the notion that the brain operates near criticality has gained considerable support, and recent work has shown that the dynamics of different brain states may be modeled by pairwise maximum entropy Ising models at various distances from a phase transition, i.e., from criticality. Here we aim to characterize two brain states (psychedelics-induced and placebo) as captured by functional magnetic resonance imaging (fMRI), with features derived from the Ising spin model formalism (system temperature, critical point, susceptibility) and from algorithmic complexity. We hypothesized, along the lines of the entropic brain hypothesis, that psychedelics drive brain dynamics into a more disordered state at a higher Ising temperature and increased complexity. We analyze resting state blood-oxygen-level-dependent (BOLD) fMRI data collected in an earlier study from fifteen subjects in a control condition (placebo) and during ingestion of lysergic acid diethylamide (LSD). Working with the automated anatomical labeling (AAL) brain parcellation, we first create "archetype" Ising models representative of the entire dataset (global) and of the data in each condition. Remarkably, we find that such archetypes exhibit a strong correlation with an average structural connectome template obtained from dMRI (r = 0.6). We compare the archetypes from the two conditions and find that the Ising connectivity in the LSD condition is lower than in the placebo one, especially in homotopic links (interhemispheric connectivity), reflecting a significant decrease of homotopic functional connectivity in the LSD condition. The global archetype is then personalized for each individual and condition by adjusting the system temperature. The resulting temperatures are all near but above the critical point of the model in the paramagnetic (disordered) phase. The individualized Ising temperatures are higher in the LSD condition than in the placebo condition (p = 9 × 10-5). Next, we estimate the Lempel-Ziv-Welch (LZW) complexity of the binarized BOLD data and the synthetic data generated with the individualized model using the Metropolis algorithm for each participant and condition. The LZW complexity computed from experimental data reveals a weak statistical relationship with condition (p = 0.04 one-tailed Wilcoxon test) and none with Ising temperature (r(13) = 0.13, p = 0.65), presumably because of the limited length of the BOLD time series. Similarly, we explore complexity using the block decomposition method (BDM), a more advanced method for estimating algorithmic complexity. The BDM complexity of the experimental data displays a significant correlation with Ising temperature (r(13) = 0.56, p = 0.03) and a weak but significant correlation with condition (p = 0.04, one-tailed Wilcoxon test). This study suggests that the effects of LSD increase the complexity of brain dynamics by loosening interhemispheric connectivity-especially homotopic links. In agreement with earlier work using the Ising formalism with BOLD data, we find the brain state in the placebo condition is already above the critical point, with LSD resulting in a shift further away from criticality into a more disordered state.