Hierarchical network structure as the source of hierarchical dynamics (power-law frequency spectra) in living and non-living systems: How state-trait continua (body plans, personalities) emerge from first principles in biophysics

Abstract

Living systems are hierarchical control systems that display a small world network structure. In such structures, many smaller clusters are nested within fewer larger ones, producing a fractal-like structure with a 'power-law' cluster size distribution (a mereology). Just like their structure, the dynamics of living systems shows fractal-like qualities: the timeseries of inner message passing and overt behavior contain high frequencies or 'states' (treble) that are nested within lower frequencies or 'traits' (bass), producing a power-law frequency spectrum that is known as a 'state-trait continuum' in the behavioral sciences. Here, we argue that the power-law dynamics of living systems results from their power-law network structure: organisms 'vertically encode' the deep spatiotemporal structure of their (anticipated) environments, to the effect that many small clusters near the base of the hierarchy produce high frequency signal changes and fewer larger clusters at its top produce ultra-low frequencies. Such ultra-low frequencies exert a tonic regulatory pressure that produces morphological as well as behavioral traits (i.e., body plans and personalities). Nested-modular structure causes higher frequencies to be embedded within lower frequencies, producing a power-law state-trait continuum. At the heart of such dynamics lies the need for efficient energy dissipation through networks of coupled oscillators, which also governs the dynamics of non-living systems (e.q., earthquakes, stock market fluctuations). Since hierarchical structure produces hierarchical dynamics, the development and collapse of hierarchical structure (e.g., during maturation and disease) should leave specific traces in system dynamics (shifts in lower frequencies, i.e. morphological and behavioral traits) that may serve as early warning signs to system failure. The applications of this idea range from (bio)physics and phylogenesis to ontogenesis and clinical medicine.

Keywords: 1/f noise; Behavior; Body-plans; Bowtie; Fourier analysis; Frequency spectra; Information bottleneck; Morphogenesis; Morphology; Network motifs; Network systems; Personality; Personality development; Phenotype; Pink noise; Power-law frequency distribution; State-trait continuum; States; Traits; Zipf’s law; active inference; adaptive radiation; allostatic overload; biophysics; cascading failure; coupled attractor systems; cross-frequency coupling; disorder; early warning signs; evolution; fractal; free energy principle; hierarchical Bayesian control systems; hub collapse; mereology; nested-modular; network dynamics; network structure; ontogenesis; permutation entropy; phase-amplitude coupling; phylogenesis; scale free; separation of timescales; small world; specialization; speciation; stress; thermodynamics.