Variability, Symmetry, and Dynamics in Human Rhythmic Motor Control (original) (raw)
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Journal of Neurophysiology, 2014
Ankarali MM, Şen HT, De A, Okamura AM, Cowan NJ. Haptic feedback enhances rhythmic motor control by reducing variability, not improving convergence rate. Stability and performance during rhythmic motor behaviors such as locomotion are critical for survival across taxa: falling down would bode well for neither cheetah nor gazelle. Little is known about how haptic feedback, particularly during discrete events such as the heelstrike event during walking, enhances rhythmic behavior. To determine the effect of haptic cues on rhythmic motor performance, we investigated a virtual paddle juggling behavior, analogous to bouncing a table tennis ball on a paddle. Here, we show that a force impulse to the hand at the moment of ball-paddle collision categorically improves performance over visual feedback alone, not by regulating the rate of convergence to steady state (e.g., via higher gain feedback or modifying the steady-state hand motion), but rather by reducing cycle-to-cycle variability. This suggests that the timing and state cues afforded by haptic feedback decrease the nervous system's uncertainty of the state of the ball to enable more accurate control but that the feedback gain itself is unaltered. This decrease in variability leads to a substantial increase in the mean first passage time, a measure of the long-term metastability of a stochastic dynamical system. Rhythmic tasks such as locomotion and juggling involve intermittent contact with the environment (i.e., hybrid transitions), and the timing of such transitions is generally easy to sense via haptic feedback. This timing information may improve metastability, equating to less frequent falls or other failures depending on the task. haptics; juggling; metastability; limit cycle; multisensory integration Address for reprint requests and other correspondence: M. M.
Complementary spatial and timing control in rhythmic arm movements
Journal of Neurophysiology
Volitional rhythmic motor behaviors such as limb cycling and locomotion exhibit spatial and timing regularity. Such rhythmic movements are executed in the presence of exogenous visual and nonvisual cues, and previous studies have shown the pivotal role that vision plays in guiding spatial and temporal regulation. However, the influence of nonvisual information conveyed through auditory or touch sensory pathways, and its effect on control, remains poorly understood. To characterize the function of nonvisual feedback in rhythmic arm control, we designed a paddle juggling task in which volunteers bounced a ball off a rigid elastic surface to a target height in virtual reality by moving a physical handle with the right hand. Feedback was delivered at two key phases of movement: visual feedback at ball peaks only and simultaneous audio and haptic feedback at ball-paddle collisions. In contrast to previous work, we limited visual feedback to the minimum required for jugglers to assess spa...
Stability and Variability in Skilled Rhythmic Action—A Dynamical Analysis of Rhythmic Ball Bouncing
Motor Control and Learning, 2006
The task of rhythmically bouncing a ball in the air serves as a model system that addresses many fundamental questions of coordination and perceptual control of actions. The task is simplified such that ball and racket movements are constrained to the vertical direction and the ball cannot be lost. As such, a discrete nonlinear model for the kinematics of periodic racket motions and ballistic ball flight between ballracket contacts was formulated which permitted a set of analyses and predictions. Most centrally, linear stability analysis predicts that the racket trajectory should be decelerating prior to ball contact in order to guarantee dynamically stable performance. Such solutions imply that small perturbations need not be explicitly corrected for and therefore provide a computationally efficient solution. Four quantitative predictions were derived from a deterministic and a stochastic version of the model and were experimentally tested. Results support that human actors sense and make use of the stability properties of task. However, when single larger perturbations arise, human actors are able to adjust their racket trajectory to correct for errors and maintain a stable bouncing pattern.
Control of bimanual rhythmic movements: trading efficiency for robustness depending on the context
Experimental Brain Research, 2008
This paper investigates how the efficiency and robustness of a skilled rhythmic task compete against each other in the control of a bimanual movement. Human subjects juggled a puck in 2D through impacts with two metallic arms, requiring rhythmic bimanual actuation. The arms kinematics were only constrained by the position, velocity and time of impacts while the rest of the trajectory did not influence the movement of the puck. In order to expose the task robustness, we manipulated the task context in two distinct manners: the task tempo was assigned at four different values (hence manipulating the time available to plan and execute each impact movement individually); and vision was withdrawn during half of the trials (hence reducing the sensory inflows). We show that when the tempo was fast, the actuation was rhythmic (no pause in the trajectory) while at slow tempo, the actuation was discrete (with pause intervals between individual movements). Moreover, the withdrawal of visual information encouraged the rhythmic behavior at the four tested tempi. The discrete versus rhythmic behavior give different answers to the efficiency/robustness trade-off: discrete movements result in energy efficient movements, while rhythmic movements impact the puck with negative acceleration, a property preserving robustness. Moreover, we report that in all conditions the impact velocity of the arms was negatively correlated with the energy of the puck. This correlation tended to stabilize the task and was influenced by vision, revealing again different control strategies. In conclusion, this task involves different modes of control that balance efficiency and robustness, depending on the context.
On rhythmic and discrete movements: reflections, definitions and implications for motor control
Experimental Brain Research, 2007
At present, rhythmic and discrete movements are investigated by largely distinct research communities using different experimental paradigms and theoretical constructs. As these two classes of movements are tightly interlinked in everyday behavior, a common theoretical foundation spanning across these two types of movements would be valuable. Furthermore, it has been argued that these two movement types may constitute primitives for more complex behavior. The goal of this paper is to develop a rigorous taxonomic foundation that not only permits better communication between different research communities, but also helps in defining movement types in experimental design and thereby clarifies fundamental questions about primitives in motor control. We propose formal definitions for discrete and rhythmic movements, analyze some of their variants, and discuss the application of a smoothness measure to both types that enables quantification of discreteness and rhythmicity. Central to the definition of discrete movement is their separation by postures. Based on this intuitive definition, certain variants of rhythmic movement are indistinguishable from a sequence of discrete movements, reflecting an ongoing debate in the motor neuroscience literature. Conversely, there exist rhythmic movements that cannot be composed of a sequence of discrete movements. As such, this taxonomy may provide a language for studying more complex behaviors in a principled fashion.
Towards an Understanding of Control of Complex Rhythmical Wavelike Coordination in Humans
How does the human neurophysiological system self-organize to achieve optimal phase relationships among joints and limbs, such as in the composite rhythms of butterfly and front crawl swimming, drumming, or dancing? We conducted a systematic review of literature relating to CNS control of phase among joint/limbs in continuous rhythmic activities. SCOPUS and Web of Science were searched using keywords ‘Phase AND Rhythm AND Coordination’. This yielded 998 matches from which 23 papers were extracted for inclusion based on screening criteria. The empirical evidence arising from in-vivo, fictive, in-vitro, and modelling of neural control in humans, other species, and robots indicates that the control of movement is facilitated and simplified by innervating muscle synergies by way of spinal central pattern generators (CPGs). These typically behave like oscillators enabling stable repetition across cycles of movements. This approach provides a foundation to guide the design of empirical re...
Rhythmic movement coordination exhibits characteristic patterns of stability, specifically that movements at 0°mean relative phase are maximally stable, 180°is stable but less so than 0°, and other coordinations are unstable without training. Recent research has demonstrated a role for perception in creating this pattern; perceptual variability judgments covary with movement variability results. This suggests that the movement results could be due in part to differential perceptual resolution of the target movement coordinations. The current study used a paradigm that enabled simultaneous access to both perception (between-trial) and movement (within-trial) stability measures. A visually specified 0°target mean relative phase enabled participants to produce stable movements when the movements were at a non-0°relationship to the target being tracked. Strong relationships were found between within-trial stability (the traditional movement measure) and between-trial stability (the traditional perceptual judgment measure), suggestive of a role for perception in producing coordination stability phenomena. The stabilization was incomplete, however, indicating that visual perception was not the sole determinant of movement stability. Rhythmic movement coordination is intrinsically a perception/action system.
Understanding Complex Systems, 2008
Since the seminal paper on phase transitions in bimanual rhythmic movements, research from the dynamical systems perspective has given primacy to rhythmic coordination. While rhythmic movements are a ubiquitous and fundamental expression in biological behavior, non-rhythmic or discrete movements are of similar importance. In fact, rhythmic and discrete movements are commonly intertwined in complex actions. This review traces our strategy of extending a dynamic systems account from rhythmic to non-rhythmic behavior. Behavioral and modeling work on uni-and bimanual, single-and multijoint coordination increasingly investigated more complex movement tasks consisting of rhythmic and discrete elements. The modeling work suggested a three-tiered architecture consisting of a biomechanical, internal and parameter level with different responsibilities for different components of movement generation. A core question raised in the modeling is what are the fundamental units and principles that are tuned to make up complex behavior. Are rhythmic pattern generators the primitives for generating both rhythmic and non-rhythmic behaviors? Alternatively, are discrete pattern generators fundamental, or are there two primitives of action? fMRI experiments compared brain activation in continuously rhythmic and discrete movements. Significantly more activation in discrete movements suggested that discrete movements have higher control demands and may be distinct primitives, different from rhythmic movements. This result corresponds to the modeling work that highlighted that discrete movements require more parameterization. Our behavioral, modeling and imaging research built on and extended the dynamical systems approach to rhythmic coordination with the goal to develop a comprehensive framework to address complex everyday actions in a principled manner.
Robotics and neuroscience: A rhythmic interaction
Neural Networks, 2008
At the crossing between motor control neuroscience and robotics system theory, the paper presents a rhythmic experiment that is amenable both to handy laboratory implementation and simple mathematical modeling. The experiment is based on an impact juggling task, requiring the coordination of two upper-limb effectors and some phase-locking with the trajectories of one or several juggled objects. We describe the experiment, its implementation and the mathematical model used for the analysis. Our underlying research focuses on the role of sensory feedback in rhythmic tasks. In a robotic implementation of our experiment, we study the minimum feedback that is required to achieve robust control. A limited source of feedback, measuring only the impact times, is shown to give promising results. A second field of investigation concerns the human behavior in the same impact juggling task. We study how a variation of the tempo induces a transition between two distinct control strategies with different sensory feedback requirements. Analogies and differences between the robotic and human behaviors are obviously of high relevance in such a flexible setup.
An integrative perspective provided by the link between biomechanics and motor control is developed in this chapter, and the implications for biomechanical modeling and measurement are discussed in detail. Running and swimming are used to examine the measurement of variability in gait under the different environmental constraints of with and without gravitational forces (swimming is viewed as an aquatic gait). The classic biomechanical method of hierarchical modeling is outlined, and components of the functional pattern of coordination used to achieve locomotion are placed in this integrated schematic to facilitate motion analysis. In analyzing the literature on running gait and overuse injuries, it is shown that variability in coordination during the interval between the initial foot contact and the neutral position of the stance phase is an important feature of normal, healthy running.