Physiological complexity: influence of ageing, disease and neuromuscular fatigue on muscle force and torque fluctuations

Abstract

New Findings What is the topic of this review?Physiological complexity in muscle force and torque fluctuations, specifically the quantification of complexity, how neuromuscular complexityis altered by perturbations and the potential mechanism underlying changes in neuromuscular complexity. What advances does it highlight?The necessity to calculate both magnitude‐ and complexity‐based measures for the thorough evaluation of force/torque fluctuations. Also the need for further research on neuromuscular complexity, particularly how it relates to the performance of functional activities (e.g. manual dexterity, balance, locomotion). Abstract Physiological time series produce inherently complex fluctuations. In the last 30 years, methods have been developed to characterise these fluctuations, and have revealed that they contain information about the function of the system producing them. Two broad classes of metrics are used: (1) those which quantify the regularity of the signal (e.g. entropy metrics); and (2) those which quantify the fractal properties of the signal (e.g. detrended fluctuation analysis). Using these techniques, it has been demonstrated that ageing results in a loss of complexity in the time series of a multitude of signals, including heart rate, respiration, gait and, crucially, muscle force or torque output. This suggests that as the body ages, physiological systems become less adaptable (i.e. the systems’ ability to respond rapidly to a changing external environment is diminished). More recently, it has been shown that neuromuscular fatigue causes a substantial loss of muscle torque complexity, a process that can be observed in a few minutes, rather than the decades it requires for the same system to degrade with ageing. The loss of torque complexity with neuromuscular fatigue appears to occur exclusively above the critical torque (at least for tasks lasting up to 30 min). The loss of torque complexity can be exacerbated with previous exercise of the same limb, and reduced by the administration of caffeine, suggesting both peripheral and central mechanisms contribute to this loss. The mechanisms underpinning the loss of complexity are not known but may be related to altered motor unit behaviour as the muscle fatigues.

Multiscale entropy analysis of retinal signals reveals reduced complexity in a mouse model of Alzheimer’s disease

“…The loss of complexity was first postulated as an age-related phenomenon such that impairment of functional components and/or altered coupling between these components would lead to a progressive decline in adaptability to physiologic stress 38 . Since then, mounting evidence in various physiological outputs showed complexity reductions with age and disease 24 , 26 , 31 , 37 , 39 . Our measurements of retinal ERG bring additional evidence of age-related loss of complexity, a feature that, in this case, emerged for diverse visual inputs.…”

“…In this case, entropy refers to signal disorder, and complexity, to the nonlinear interactions between various structural units and their collective behavior, operating over a wide range of temporal and spatial scales 23 . Physiological complexity has received increased attention due to the theory of complexity-loss with aging and disease 23 – 26 . This theory postulates that, as stated by Goldberger et al 24 : 1) “the output of healthy systems (...) reveals a type of complex variability associated with long-range correlations”, and 2) “this type of multiscale, nonlinear complexity breaks down with aging and disease, reducing the adaptive capabilities of the individual”.…”

Multiscale Entropy Analysis of Retinal Signals Reveals Reduced Complexity in a Mouse Model of Alzheimer’s Disease

“…The loss of complexity was first postulated as an age-related phenomenon such that impairment of functional components and/or altered coupling between these components would lead to a progressive decline in adaptability to physiologic stress 38 . Since then, mounting evidence in various physiological outputs showed complexity reductions with age and disease 24,26,31,37,39 . Our measurements of retinal µERG bring additional evidence of age-related loss of complexity, a feature that, in this case, emerged for diverse visual inputs.…”

“…In this case, entropy refers to signal disorder, and complexity, to the nonlinear interactions between various structural units and their collective behavior, operating over a wide range of temporal and spatial scales 23 . Physiological complexity has received increased attention due to the theory of complexity-loss with aging and disease [23][24][25][26] . This theory postulates that, as stated by Goldberger et al 24 : 1) "the output of healthy systems (...) reveals a type of complex variability associated with long-range correlations", and 2) "this type of multiscale, nonlinear complexity breaks down with aging and disease, reducing the adaptive capabilities of the individual".…”

The effect of breaking up sedentary time with calisthenics on neuromuscular function: a preliminary study

“…Magnitude-based measures of force control characterise force steadiness, while complexitybased measures reflect force adaptability; that is, the ability to modulate force output rapidly and accurately in response to task demands (Pethick et al, 2021b).…”