Complex systems approaches to the adaptability of human functions and behavior in health, aging, and chronic diseases: protocol for a meta-narrative review.

BACKGROUND: Evaluating the adaptability of human functions and behavior has become a subject of growing interest due to aging populations and the increased prevalence of chronic diseases. Various research traditions, based on complex systems theories, have addressed the adaptability of human functions and behavior. However, despite the different research traditions, no review has so far compared them to provide a reliable and useful synthetic tool. Based on an adapted methodology, study objectives are to refine common and divergent traits in the way adaptability of the human functions and behavior has been studied via complex system approaches, with a special focus on aging and chronic diseases. In order to meet this objective, we will use the methodology of the meta-narrative review, and we present in this article the protocol that we will follow. METHODS: The meta-narrative review explores the contrasting and complementary ways in which researchers have studied a subject in order to synthesize information and extract theoretical and applied recommendations. In order to carry out this protocol, we detail our methodology of article extraction, coding, and synthesis. We present the six main stages of our review, from the planning stage to the recommendation stage, and the way we will implement the six principles that underpin the construction of a meta-narrative review. DISCUSSION: The use of a meta-narrative review methodology will yield greater visibility and comprehension of the adaptability of human functions and behavior studied via complex systems-based approaches. In a broader perspective, this paper is also geared to help future researchers carry out a meta-narrative review by highlighting the main challenges encountered and anticipated as well as elements to be taken into account before starting such a project.

Relationship between gait complexity and pain attention in chronic low back pain.

ABSTRACT: Clinical models of chronic low back pain (cLBP) highlight the role of excessive attention to pain and kinesiophobia on the origin of disability. At the motor control level, various mechanisms are involved in the impairments observed in patients with cLBP. We aimed to assess the role of maladaptative attentional behaviors by using a complex systems approach and a visual display as a distraction during walking. Sixteen patients with cLBP with no previous surgery or significant leg pain and 16 healthy matched controls were included. Patients walked on a treadmill at preferred walking speed with and without distraction. Stride time (ST) fractal complexity was assessed using detrended fluctuation analysis. A two-way analysis of variance with repeated measures on distraction was performed on fractal exponents. We found a significant group × distraction interaction effect on fractal complexity of ST series (F(1,30) = 9.972, P = 0.004). Post hoc analysis showed that, without distraction, patients with cLBP had significantly lower ST complexity than controls, but when distracted, they regained gait complexity, recovering the level of controls. Our results suggest that excessive attention to pain causes loss of complexity and adaptability in cLBP and explain alterations of motor control with pain. Fractal analysis seems to be a promising method to explore movement variability and individual adaptability in musculoskeletal disorders.

Adaptive Capacities and Complexity of Heart Rate Variability in Patients With Chronic Obstructive Pulmonary Disease Throughout Pulmonary Rehabilitation.

INTRODUCTION: The complexity of bio-signals, like R-R intervals, is considered a reflection of the organism's capacity to adapt. However, this association still remains to be consolidated. We investigated whether the complexity of R-R intervals at rest and during perturbation [6-minute walking test (6MWT)], yielded information regarding adaptive capacities in Chronic Obstructive Pulmonary Disease (COPD) patients during pulmonary rehabilitation (PR). METHODS: In total, 23 COPD patients (64 ± 8 years, with forced expiratory volume in 1 s of 55 ± 19% predicted) were tested three times at the start (T1), middle (T2), and end (T3) of 4 weeks PR. Each time, R-R intervals were measured at rest and during 6MWT. The complexity of R-R intervals was assessed by evenly spaced Detrended Fluctuations Analysis and evaluated by the fractal exponent α and deviation from maximal complexity |1-α|. RESULTS: The 6MWT distance was significantly increased at T2 and T3 compared to T1. Neither α nor |1-α| at rest and during perturbation significantly changed throughout PR, nor were they consistently associated with 6MWT distances at each time. Throughout the PR program, complexity during the 6MWT was significantly lower compared to the rest. The level of α during 6MWT at T1 was positively correlated with the improvement of the 6MWT distance throughout the PR program. DISCUSSION: Reduced complexity in COPD patients during acute perturbation at the beginning of PR supports a decreased improvement of the 6MWT distance throughout PR. This result seems consistent with the notion that the complexity reflects the patients' adaptive capacities and could therefore become a clinical indicator in an applied perspective.

Fractal properties in sensorimotor variability unveil internal adaptations of the organism before symptomatic functional decline.

If health can be defined as adaptability, then measures of adaptability are crucial. Convergent findings across clinical areas established the notion that fractal properties in bio-behavioural variability characterize the healthy condition of the organism, and its adaptive capacities in general. However, ambiguities remain as to the significance of fractal properties: the literature mainly discriminated between healthy vs. pathological states, thereby loosing perspective on the progression in between, and overlooking the distinction between adaptability and effective adaptations of the organism. Here, we design an experimental tapping paradigm involving gradual feedback deprivation in groups of healthy subjects and one deafferented man as a pathological-limit case. We show that distinct types of fractal properties in sensorimotor behaviour characterize, on the one hand impaired functional ability, and on the other hand internal adaptations for maintaining performance despite the imposed constraints. Findings may prove promising for early detection of internal adaptations preceding symptomatic functional decline.

Concurrent Changes of Brain Functional Connectivity and Motor Variability When Adapting to Task Constraints.

In behavioral neuroscience, the adaptability of humans facing different constraints has been addressed on one side at the brain level, where a variety of functional networks dynamically support the same performance, and on the other side at the behavioral level, where fractal properties in sensorimotor variables have been considered as a hallmark of adaptability. To bridge the gap between the two levels of observation, we have jointly investigated the changes of network connectivity in the sensorimotor cortex assessed by modularity analysis and the properties of motor variability assessed by multifractal analysis during a prolonged tapping task. Four groups of participants had to produce the same tapping performance while being deprived from 0, 1, 2, or 3 sensory feedbacks simultaneously (auditory and/or visual and/or tactile). Whereas tapping performance was not statistically different across groups, the number of brain networks involved and the degree of multifractality of the inter-tap interval series were significantly correlated, increasing as a function of feedback deprivation. Our findings provide first evidence that concomitant changes in brain modularity and multifractal properties characterize adaptations underlying unchanged performance. We discuss implications of our findings with respect to the degeneracy properties of complex systems, and the entanglement of adaptability and effective adaptation.

Dynamics of the human brain network revealed by time-frequency effective connectivity in fNIRS.

Functional near infrared spectroscopy (fNIRS) is a promising neuroimaging method for investigating networks of cortical regions over time. We propose a directed effective connectivity method (TPDC) allowing the capture of both time and frequency evolution of the brain's networks using fNIRS data acquired from healthy subjects performing a continuous finger-tapping task. Using this method we show the directed connectivity patterns among cortical motor regions involved in the task and their significant variations in the strength of information flow exchanges. Intra and inter-hemispheric connections during the motor task with their temporal evolution are also provided. Characterisation of the fluctuations in brain connectivity opens up a new way to assess the organisation of the brain to adapt to changing task constraints, or under pathological conditions.

Expectations induced by natural-like temporal fluctuations are independent of attention decrement: evidence from behavior and early visual evoked potentials.

Temporal expectations and attention decrement affect human behavior in opposing ways: the former positively, the latter negatively yet both exhibit similar neural signatures - i.e., reduction in the early event-related potential components' amplitude - despite different underlying mechanisms. Furthermore, there is a significant and growing debate in the literature regarding the putative role of attention in the encoding of expectations in perception. The question then arises as to what are the behavioral and neural consequences, if any, of attention decrement on temporal expectations and related enhancement of sensory information processing. Here, we investigated behavioral performance and visual N1a, N1p and P1 components during a sustained attention reaction time task inducing attention decrement under two conditions. In one condition, the inter-stimulus intervals (ISIs) were randomly distributed to impede expectation effects while for the other, the ISI exhibited natural-like long-term correlations supposed to induce temporal expectations. Behavioral results show that natural-like fluctuations in ISI indeed induced faster RT due to temporal expectations. These temporal expectations were beneficial even under attention decrement circumstances. Further, temporal expectations were associated with reduced N1a amplitude while attention decrement was associated with reduced N1p amplitude. Our findings provide evidence that the effects of temporal expectations and attention decrement induced in a single task can be independent at the behavioral level, and are supported at separate information processing stages at the neural level in vision.

Persistent fluctuations in stride intervals under fractal auditory stimulation.

Stride sequences of healthy gait are characterized by persistent long-range correlations, which become anti-persistent in the presence of an isochronous metronome. The latter phenomenon is of particular interest because auditory cueing is generally considered to reduce stride variability and may hence be beneficial for stabilizing gait. Complex systems tend to match their correlation structure when synchronizing. In gait training, can one capitalize on this tendency by using a fractal metronome rather than an isochronous one? We examined whether auditory cues with fractal variations in inter-beat intervals yield similar fractal inter-stride interval variability as isochronous auditory cueing in two complementary experiments. In Experiment 1, participants walked on a treadmill while being paced by either an isochronous or a fractal metronome with different variation strengths between beats in order to test whether participants managed to synchronize with a fractal metronome and to determine the necessary amount of variability for participants to switch from anti-persistent to persistent inter-stride intervals. Participants did synchronize with the metronome despite its fractal randomness. The corresponding coefficient of variation of inter-beat intervals was fixed in Experiment 2, in which participants walked on a treadmill while being paced by non-isochronous metronomes with different scaling exponents. As expected, inter-stride intervals showed persistent correlations similar to self-paced walking only when cueing contained persistent correlations. Our results open up a new window to optimize rhythmic auditory cueing for gait stabilization by integrating fractal fluctuations in the inter-beat intervals.

'Human paced' walking: followers adopt stride time dynamics of leaders.

Isochronous cueing is widely used in gait rehabilitation even though it alters the stride-time dynamics toward anti-persistent rather than the persistent, fractal fluctuations characteristic of human walking. In the present experiment we tested an alternative cueing method: pacing by a human. To this end, we formed sixteen pairs of walkers based on their preferred stride frequency. Each pair consisted of a designated "leader" and a "follower" who was instructed to synchronize his or her steps to those of the leader. Heel strike times were detected with tiny footswitches, and Detrended Fluctuation Analysis (DFA) was applied to estimate fractal exponents of stride-time series. To ensure that the stride-time dynamics of the follower matched those of the leader, the latter was structurally modified by artificial cueing via either an isochronous metronome or a fractal metronome, in contrast to self-paced walking. Mean relative phases between followers and leaders were close to 0°, confirming that followers effectively synchronized their footfalls with those of the leaders. Mean fractal exponents were not statistically different between followers and leaders in any condition and highly correlated, suggesting that followers matched their stride-time structure to that of leaders. Our results open perspectives for alternative, more natural cueing protocols for gait rehabilitation.

Asymmetries of bilateral isometric force matching with movement intention and unilateral fatigue.

During bilateral coordination, some level of inter-hemispheric remapping (i.e., the congruency between afferent and efferent force signals from both hemispheres) is required. In this case, sensory-motor information is exchanged between the two hemispheres, but it remains unclear whether this information exchange is always equivalent or not, especially in a bilateral isometric force-matching task. We used unilateral fatigue applied to one arm in order to determine whether inter-hemispheric remapping can vary asymmetrically during a bilateral isometric matching task. Because fatigue is considered to bias the sensory-motor system, we hypothesized that if bimanual coordination is modulated solely in function of the state of the sensory-motor system (motor efferences, inter-hemispheric inhibitions, and sensory reafferences), we should not observe any asymmetric effect of fatigue with movement intention (leading vs. matching arm). However, if any other process could participate in the modulation of inter-hemispheric remapping, we should observe an interaction between movement intentions and fatigue on the force produced. We found that, when the leading arm was the non-fatigued arm, participants succeeded in reproducing the force level with their fatigued arm. By contrast, when the leading arm was fatigued, subjects over-estimated the force level produced with their non-fatigued arm. Hence, lateralized fatigue exacerbates an asymmetric behavior that seems modulated by movement intention (leading vs. matching). In other words, when unilateral fatigue is introduced in a bilateral isometric force-matching task, inter-hemispheric remapping is asymmetrical. Intensity levels of motor commands sent to both arms (directly or modulated through inter-hemispheric inhibitions) and sensory reafferences alone cannot explain these observations. Some attentional focus may be not balanced continuously between both arms but may be mainly directed toward the matching arm.

Predicting the biological variability of environmental rhythms: weak or strong anticipation for sensorimotor synchronization?

The internal processes involved in synchronizing our movements with environmental stimuli have traditionally been addressed using regular metronomic sequences. Regarding real-life environments, however, biological rhythms are known to have intrinsic variability, ubiquitously characterized as fractal long-range correlations. In our research we thus investigate to what extent the synchronization processes drawn from regular metronome paradigms can be generalized to other (biologically) variable rhythms. Participants performed synchronized finger tapping under five conditions of long-range and/or short-range correlated, randomly variable, and regular auditory sequences. Combining experimental data analysis and numerical simulation, we found that synchronizing with biologically variable rhythms involves the same internal processes as with other variable rhythms (whether totally random or comprising lawful regularities), but different from those involved with a regular metronome. This challenges both the generalizability of conclusions drawn from regular-metronome paradigms, and recent research assuming that biologically variable rhythms may trigger specific strong anticipatory processes to achieve synchronization.

Somatosensory-related limitations for bimanual coordination after stroke.

BACKGROUND: Bimanual coordinated movements may be impaired after stroke, so an assessment of causes is necessary to optimize rehabilitation strategies. OBJECTIVE: We assessed the role of afference-based sources of coordination, including phase entrainment and error correction based on visual and somatosensory feedback. METHODS: In all, 10 persons with unilateral chronic stroke and 8 age-matched controls participated in a kinesthetic tracking protocol, in which the hemiparetic upper limb was passively driven by the machine. The task consisted of matching the trajectory of the driven limb as accurately as possible with the freely moving limb in 2 conditions: eyes closed and eyes open. We analyzed the continuous relative phase (CRP), the mean absolute difference between positions (ADP) between the positions of the 2 limbs, and the jerk of the matching limb. RESULTS: Coordination instability (CRP standard deviation) and mean ADP were significantly higher for patients with eyes closed, compared with patients with eyes open, controls with eyes closed, and controls with eyes open. Moreover, the jerk was higher for the nonparetic limb of patients than for the control group. Thus, the nonparetic limb did not produce optimally smooth movements even as the motor-driven paretic limb did. CONCLUSION: Besides deficits caused by interhemispheric competition and motor execution of the paretic limb, somatosensory feedback is a limiting factor in bimanual coordination after stroke. The findings have clinical implications pertaining to the design and individualization of efficient bimanual movement therapy.

Changes in bimanual coordination during the first 6 weeks after moderate hemiparetic stroke.

BACKGROUND: Better understanding of how bimanual coordination changes over the first weeks of recovery after stroke is required to address the potential utility for bimanual rehabilitation. Three-dimensional kinematic analysis can provide quantitative assessment of unimanual and bimanual movements. OBJECTIVE: To assess the natural evolution of reaching kinematics during standard poststroke rehabilitation, focusing on bimanual coordination. METHODS: A total of 12 hemiparetic, moderately impaired patients were included within 30 days after a first unilateral ischemic/hemorrhagic stroke; 7 kinematic assessments were performed once a week for 6 weeks and at 3 months after inclusion. The reach-to-grasp task was performed in 3 different conditions: unimanual with the healthy limb (UN), unimanual with the paretic limb (UP), and bimanual (BN/BP). RESULTS: For the paretic limb, movement fluency (number of movement units and total movement time) was lower for bimanual reaching compared with unimanual reaching. For bimanual reaching, (1) movement kinematics were similar for both limbs, (2) recovery patterns of both limbs followed a similar profile with a plateau phase at 6 weeks poststroke, and (3) intertrial variability of between-hands synchronization decreased over sessions, although the mean delays remained the same. CONCLUSIONS: Bimanual coordination started to become efficient 6 weeks after onset of stroke, so for patients such as those we tested, this time could be most opportune to start bimanual-oriented rehabilitation. The challenge in future research includes determining the characteristics of patients who may best benefit from bimanual therapy.

Relative roughness: an index for testing the suitability of the monofractal model.

Fractal analyses have become very popular and have been applied on a wide variety of empirical time series. The application of these methods supposes that the monofractal framework can offer a suitable model for the analyzed series. However, this model takes into account a quite specific kind of fluctuations, and we consider that fractal analyses have been often applied to series that were completely outside of its relevance. The problem is that fractal methods can be applied to all types of series, and they always give a result, that one can then erroneously interpret in the context of the monofractal framework. We propose in this paper an easily computable index, the relative roughness (RR), defined as the ratio between local and global variances, that allows to test for the applicability of fractal analyses. We show that RR is confined within a limited range (between 1.21 and 0.12, approximately) for long-range correlated series. We propose some examples of empirical series that have been recently analyzed using fractal methods, but, with respect to their RR, should not have been considered in the monofractal model. An acceptable level of RR, however, is a necessary but not sufficient condition for considering series as long-range correlated. Specific methods should be used in complement for testing for the effective presence of long-range correlations in empirical series.

Complexity in neurobiology: perspectives from the study of noise in human motor systems.

This article serves as an introduction to the themed special issue on "Complex Systems in Neurobiology." The study of complexity in neurobiology has been sensitive to the stochastic processes that dominate the micro-level architecture of neurobiological systems and the deterministic processes that govern the macroscopic behavior of these systems. A large body of research has traversed these scales of interest, seeking to determine how noise at one spatial or temporal scale influences the activity of the system at another scale. In introducing this special issue, we pay special attention to the history of inquiry in complex systems and why scientists have tended to favor linear, causally driven, reductionist approaches in Neurobiology. We follow this with an elaboration of how an alternative approach might be formulated. To illustrate our position on how the sciences of complexity and the study of noise can inform neurobiology, we use three systematic examples from the study of human motor control and learning: 1) phase transitions in bimanual coordination; 2) balance, intermittency, and discontinuous control; and 3) sensorimotor synchronization and timing. Using these examples and showing that noise is adaptively utilized by the nervous system, we make the case for the studying complexity with a perspective of understanding the macroscopic stability in biological systems by focusing on component processes at extended spatial and temporal scales. This special issue continues this theme with contributions in topics as diverse as neural network models, physical biology, motor learning, and statistical physics.

Event-based and emergent timing: dichotomy or continuum? A reply to Repp and Steinman (2010).

B. H. Repp and S. R. Steiman (2010) suggested that event-based and emergent timing, usually conceived as mutually exclusive modes of timing, could in fact coexist in a single activity. According to this point of view, rhythmic activities could exploit mixtures of control modes, in which the relative importance of event-based and emergent components could depend on task characteristics. This point of view, in the opinion of the authors of the present article, corresponds to a fundamental misunderstanding of the theoretical basis of the event-based and emergent distinction, and is not supported by any experimental evidence. However, they present some new results that could support new lines of reasoning for the future developments of research in this domain.

Transition from persistent to anti-persistent correlations in postural sway indicates velocity-based control.

The displacement of the center-of-pressure (COP) during quiet stance has often been accounted for by the control of COP position dynamics. In this paper, we discuss the conclusions drawn from previous analyses of COP dynamics using fractal-related methods. On the basis of some methodological clarification and the analysis of experimental data using stabilogram diffusion analysis, detrended fluctuation analysis, and an improved version of spectral analysis, we show that COP velocity is typically bounded between upper and lower limits. We argue that the hypothesis of an intermittent velocity-based control of posture is more relevant than position-based control. A simple model for COP velocity dynamics, based on a bounded correlated random walk, reproduces the main statistical signatures evidenced in the experimental series. The implications of these results are discussed.

Long-range correlation properties in motor timing are individual and task specific.

1/f (ß) noise represents a specific form of (long-range) correlations in a time series that is pervasive across many sensorimotor variables. Recent studies have shown that the precise properties of the correlations demonstrated by a group of test participants may vary as a function of experimental conditions or factors characterizing the group. Our purpose in the present study was to clarify whether long-range correlations affect sensorimotor performance generally or in a task-specific manner and whether each individual produces characteristic long-range correlations that are reliable across several runs of the same task. We analyzed the series of time intervals produced by 43 participants in two timing tasks: unimanual rhythmic tapping and circle drawing. We found that a participant's 1/f (ß) properties in tapping were not related to the 1/f (ß) properties in circle drawing. However, within each task, individual differences were reliable, and a Cronbach's alpha of .59 showed a high degree of within-subjects reproducibility of the long-range correlations. Thus, long-range correlations represent a consistent and distinctive characteristic of individuals performing a particular task, rather than a ubiquitous generic property of sensorimotor time series. The implications of these results are discussed from both a theoretical and a methodological perspective.

Contemporary theories of 1/f noise in motor control.

1/f noise has been discovered in a number of time series collected in psychological and behavioral experiments. This ubiquitous phenomenon has been ignored for a long time and classical models were not designed for accounting for these long-range correlations. The aim of this paper is to present and discuss contrasted theoretical perspectives on 1/f noise, in order to provide a comprehensive overview of current debates in this domain. In a first part, we propose a formal definition of the phenomenon of 1/f noise, and we present some commonly used methods for measuring long-range correlations in time series. In a second part, we develop a theoretical position that considers 1/f noise as the hallmark of system complexity. From this point of view, 1/f noise emerges from the coordination of the many elements that compose the system. In a third part, we present a theoretical counterpoint suggesting that 1/f noise could emerge from localized sources within the system. In conclusion, we try to draw some lines of reasoning for going beyond the opposition between these two approaches.