Genetic polymorphisms in COMT and BDNF influence synchronization dynamics of human neuronal oscillations

Simola, Jaana; Siebenhühner, Felix; Myrov, Vladislav; Kantojärvi, Katri; Paunio, Tiina; Brattico, Elvira; Palva, Satu

doi:10.1016/j.isci.2022.104985

Cited by 6 publications

(14 citation statements)

References 117 publications

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“…Importantly excitation-inhibition (E/I) (E/I ratio) is the main control parameter of critical dynamics such that it emerges at E/I balance, while excess inhibition or excitation leads to sub-or super-critical dynamics, respectively [85][86][87][88][89][90][91] . In line with this framework, LRTCs are influenced by pharmacological modulations of neuronal excitability [92][93][94][95] as well as by polymorphism in neuromodulatory genes 96 . Aberrant LRTCs in ADHD could hence arise via mechanisms that influence the E/I ratio at the systems level or in specific neuronal circuits.…”

Section: Discussionmentioning

confidence: 89%

Is mild ADHD beneficial: Brain criticality is maximal with moderate ADHD symptom scores

Hirvonen

Haque

Wang

et al. 2022

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Attention-deficit/hyperactivity disorder (ADHD) is characterized by involuntary fluctuations of attention in continuous performance tasks (CPTs) wherein attention must be sustained over long periods of time. The neuronal basis underlying aberrant attentional fluctuations in time scales from seconds to minutes have remained poorly understood. Neuronal alpha- and gamma-band oscillations are thought to implement attentional and top-down control of sensorimotor processing. We hypothesized that aberrant behavioral fluctuations in ADHD would be caused by aberrant endogenous brain dynamics in alpha and gamma-band oscillations and specifically by their aberrant long-range temporal correlations (LRTCs). We measured brain activity with magnetoencephalography (MEG) from adult participants diagnosed with ADHD (N = 19) and from healthy control subjects (N = 20) during resting state and two CPTs; a threshold stimulus detection task and a Go/NoGo task. We then estimated LRTCs of neuronal oscillations and behavioral fluctuations with detrended fluctuation analysis (DFA). ADHD was associated with aberrant LRTCs in both behavioral performance and of neuronal oscillations. LRTCs were correlated with symptom severity with a U-shaped correlations indicating that the LRTCs were largest with moderate symptom scores. These data demonstrate the presence of aberrant temporal dynamics of neuronal oscillations in adult ADHD patients, which may underlie involuntary attentional fluctuations in ADHD. Taken that LRTCs are a hallmark of brain critical dynamics, these data show that moderate ADHD symptoms scores maximize brain criticality which is thought to be beneficial for performance.

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Section: Discussionmentioning

confidence: 89%

Is mild ADHD beneficial: Brain criticality is maximal with moderate ADHD symptom scores

Hirvonen

Haque

Wang

et al. 2022

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“…As both connectivity and LRTCs are test-retest reliable (Candelaria-Cook et al, 2022;Nikulin & Brismar, 2004;Wiesman et al, 2022), heritable (Leppäaho et al, 2019;Linkenkaer-Hansen et al, 2007;Nikulin & Brismar, 2005), and influenced by genetic polymorphisms (Simola et al, 2022), we postulate that the individual's position in the critical regime is a phenotypic trait that predicts individuals' brain dynamics and behaviors. We postulate that individual variability in critical dynamics could underlie variability in cognitive abilities and personality traits (J. M. Palva et al, 2013) given that operating at critical dynamics is thought to maximize the dynamic range of the system, sensitivity to external and internal perturbations, transmission, storage, and computational capacity (Beggs et al, 2007;Chialvo, 2010;Larremore et al, 2011;S.…”

Section: Discussionmentioning

confidence: 94%

“…We first used computational modelling to assess how the correlations of large-scale synchronization and LRCTs are determined by the operating point in the critical regime. We modelled local and large-scale neuronal oscillatory dynamics with a nested variant (Siebenhühner et al, 2020) of the Kuramoto model (Simola et al, 2022) with 100 regions containing 500 oscillators each. In this model coupling parameters K and L control the intra- and inter-regional, respectively, coupling strengths.…”

Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

“…Synchronization and LRTCs are aberrant also in multiple brain other diseases (Ajramj et al, 2017; Auno et al, 2021; Bajo et al, 2012; Bartolomei et al, 2013; Bruining et al, 2020; Linkenkaer-Hansen et al, 2005; Meisel et al, 2015; Monto et al, 2007; Parish et al, 2004; Pusil et al, 2019; Smit et al, 2011; Uhlhaas et al, 2006). Taken that brain criticality is primarily thought to be controlled by the E/I ratio, where an imbalance of E/I or connectivity leads to sub- or super-critical dynamics being modulated by polymorphism in neuromodulatory genes (Plenz & Thiagarajan, 2007; Poil et al, 2012; Shew et al, 2009, 2011; Simola et al, 2022) and that pathological human brain activity is associated with changes in brain E/I balance (Bajo et al, 2012; Pusil et al, 2019; Uhlhaas et al, 2006), pathological synchronization dynamics (hypo- or hyperconnectivity) could emerge via modulations of brain critical dynamics.…”

Section: Discussionmentioning

confidence: 99%

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Brain criticality predicts individual synchronization levels in humans

Fuscà

Siebenhühner

Wang

et al. 2022

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Moderate levels of synchronization of neuronal oscillations are essential for healthy brain dynamics. Synchronization levels exhibit large inter-individual variability the origins of which are unknown. Neuronal systems have been postulated to operate near a critical transition point or in an extended regime between disorder (subcritical) and order (supercritical phase) characterized by moderate synchronization and emergent power-law long-range temporal correlations (LRTCs). We investigated whether inter-individual variability in synchronization levels is explained by the individual position along the critical regime by analyzing magnetoencephalography (MEG) and intra-cerebral stereo-electroencephalography (SEEG) human resting-state data. Here we show that variability in synchronization levels exhibits a positive linear and quadratic relationships with LRTCs in healthy participants and brain areas. In the epileptogenic zone this correlation was negative. These results show that variability in synchronization levels is regulated by the individual position along an extended critical-like regime, with healthy brain areas tending to operate in its subcritical and epileptogenic areas in its supercritical side.

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Brain criticality predicts individual levels of inter-areal synchronization in human electrophysiological data

et al. 2023

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Neuronal oscillations and their synchronization between brain areas are fundamental for healthy brain function. Yet, synchronization levels exhibit large inter-individual variability that is associated with behavioral variability. We test whether individual synchronization levels are predicted by individual brain states along an extended regime of critical-like dynamics – the Griffiths phase (GP). We use computational modelling to assess how synchronization is dependent on brain criticality indexed by long-range temporal correlations (LRTCs). We analyze LRTCs and synchronization of oscillations from resting-state magnetoencephalography and stereo-electroencephalography data. Synchronization and LRTCs are both positively linearly and quadratically correlated among healthy subjects, while in epileptogenic areas they are negatively linearly correlated. These results show that variability in synchronization levels is explained by the individual position along the GP with healthy brain areas operating in its subcritical and epileptogenic areas in its supercritical side. We suggest that the GP is fundamental for brain function allowing individual variability while retaining functional advantages of criticality.

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Genetic polymorphisms in COMT and BDNF influence synchronization dynamics of human neuronal oscillations

Cited by 6 publications

References 117 publications

Is mild ADHD beneficial: Brain criticality is maximal with moderate ADHD symptom scores

Is mild ADHD beneficial: Brain criticality is maximal with moderate ADHD symptom scores

Brain criticality predicts individual synchronization levels in humans

Brain criticality predicts individual levels of inter-areal synchronization in human electrophysiological data

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