Toy-oriented changes in early arm movements III: constraints on joint kinematics

The purpose of this study was to identify invariant features of shoulder and elbow kinematics during prereaching arm movements with and without a toy present. Invariant movement features may reflect the presence of constraints that reduce the complexity of learning to reach and provide a link between early arm movements and reaching. Joint excursion and smoothness were consistently greater at the shoulder than the elbow suggesting strong organismal constraints on prereaching movements. Speed became greater in the shoulder than the elbow only with a toy present during the 4 weeks leading up to reach onset suggesting the introduction of task related constraints. We propose that organismal constraints on joint coordination throughout the prereaching period provide a foundation for the overlay of task related constraints closer to reach onset. We also suggest that the coordinative structures of early arm movements and later reaching may be much more similar than currently thought. This similarity would significantly reduce the elements needing to be actively controlled, and simplify the learning process.     

Exploiting redundancy for flexible behavior: unsupervised learning in a modular sensorimotor control architecture

Autonomously developing organisms face several challenges when learning reaching movements. First, motor control is learned unsupervised or self-supervised. Second, knowledge of sensorimotor contingencies is acquired in contexts in which action consequences unfold in time. Third, motor redundancies must be resolved. To solve all 3 of these problems, the authors propose a sensorimotor, unsupervised, redundancy-resolving control architecture (SURE_REACH), based on the ideomotor principle. Given a 3-degrees-of-freedom arm in a 2-dimensional environment, SURE_REACH encodes 2 spatial arm representations with neural population codes: a hand end-point coordinate space and an angular arm posture space. A posture memory solves the inverse kinematics problem by associating hand end-point neurons with neurons in posture space. An inverse sensorimotor model associates posture neurons with each other action-dependently. Together, population encoding, redundant posture memory, and the inverse sensorimotor model enable SURE_REACH to learn and represent sensorimotor grounded distance measures and to use dynamic programming to reach goals efficiently. The architecture not only solves the redundancy problem but also increases goal reaching flexibility, accounting for additional task constraints or realizing obstacle avoidance. While the spatial population codes resemble neurophysiological structures, the simulations confirm the flexibility and plausibility of the model by mimicking previously published data in arm-reaching tasks.     

Sensorimotor intentionality: The origins of intentionality in prospective agent action

Efficient prospective motor control, evident in human activity from birth, reveals an adaptive intentionality of a primary, pre-reflective, and pre-conceptual nature that we identify here as sensorimotor intentionality. We identify a structural continuity between the emergence of this earliest form of prospective movement and the structure of mental states as intentional or content-directed in more advanced forms. We base our proposal on motor control studies, from foetal observations through infancy. These studies reveal movements are guided by anticipations of future effects, even from before birth. This implies that these movements, even if they are simple and discrete, are the actions of an intentional agent. We develop this notion to present a theory of the developing organisation of a core feature of cognition as embodied agent action, from early single actions with proximal prospectivity to the complex serial ordering of actions into projects to reach distal goals. We claim the prospective structural continuity from early and simple actions to later complex projects of serially-ordered actions confirms the existence of an ontogenetically primary form of content–directedness that is a driver for learning and development. Its implications for understanding autism are discussed.     

Baby steps: investigating the development of perceptual–motor couplings in infancy

There are cells in our motor cortex that fire both when we perform and when we observe similar actions. It has been suggested that these perceptual‐motor couplings in the brain develop through associative learning during correlated sensorimotor experience. Although studies with adult participants have provided support for this hypothesis, there is no direct evidence that associative learning also underlies the initial formation of perceptual–motor couplings in the developing brain. With the present study we addressed this question by manipulating infants’ opportunities to associate the visual and motor representation of a novel action, and by investigating how this influenced their sensorimotor cortex activation when they observed this action performed by others. Pre‐walking 7–9‐month‐old infants performed stepping movements on an infant treadmill while they either observed their own real‐time leg movements (Contingent group) or the previously recorded leg movements of another infant (Non‐contingent control group). Infants in a second control group did not perform any steps and only received visual experience with the stepping actions. Before and after the training period we measured infants’ sensorimotor alpha suppression, as an index of sensorimotor cortex activation, while they watched videos of other infants’ stepping actions. While we did not find greater sensorimotor alpha suppression following training in the Contingent group as a whole, we nevertheless found that the strength of the visuomotor contingency experienced during training predicted the amount of sensorimotor alpha suppression at post‐test in this group. We did not find any effects of motor experience alone. These results suggest that the development of perceptual–motor couplings in the infant brain is likely to be supported by associative learning during correlated visuomotor experience.     

Imitation in infancy: the wealth of the stimulus

Imitation requires the imitator to solve the correspondence problem--to translate visual information from modelled action into matching motor output. It has been widely accepted for some 30 years that the correspondence problem is solved by a specialized, innate cognitive mechanism. This is the conclusion of a poverty of the stimulus argument, realized in the active intermodal matching model of imitation, which assumes that human neonates can imitate a range of body movements. An alternative, wealth of the stimulus argument, embodied in the associative sequence learning model of imitation, proposes that the correspondence problem is solved by sensorimotor learning, and that the experience necessary for this kind of learning is provided by the sociocultural environment during human development. In a detailed and wide-ranging review of research on imitation and imitation-relevant behaviour in infancy and beyond, we find substantially more evidence in favour of the wealth argument than of the poverty argument.     

The influence of environmental context in interpersonal observation–execution

Cyclical upper-limb movements involuntarily deviate from a primary movement direction when the actor concurrently observes incongruent biological motion. We examined whether environmental context influences such motor interference during interpersonal observation–execution. Participants executed continuous horizontal arm movements while observing congruent horizontal or incongruent curvilinear biological movements with or without the presence of an object positioned as an obstacle or distractor. When participants were observing a curvilinear movement, an object located within the movement space became an obstacle, and, thus, the curvilinear trajectory was essential to reach into horizontal space. When acting as a distractor, or with no object, the curvilinear trajectory was no longer essential. For observing horizontal movements, objects were located at the same relative locations as in the curvilinear movement condition. We found greater involuntary movement deviation when observing curvilinear than horizontal movements. Also, there was an influence of context only when observing horizontal movements, with greater deviation exhibited in the presence of a large obstacle. These findings suggest that the influence of environmental context is underpinned by the (mis-)matching of observed and executed actions as incongruent biological motion is primarily coded via bottom-up sensorimotor processes, whilst the congruent condition incorporates surrounding environmental features to modulate the bottom-up sensorimotor processes.     

The development and learning of the visual control of movement: An ecological perspective

We compare development and learning of the visual control of movement from an ecological perspective. It is argued that although the constraints that are imposed upon development and learning are vastly different, both are best characterised as a change towards the use of more useful and specifying optic variables. Implicit learning, in which awareness is drawn away from movement execution, is most appropriate to accomplish this change in optic variable use, although its contribution in development is more contentious. Alternatively, learning can also be affected by explicit processes. We propose that explicit learning would typically invoke vision for perception processes instead of the designated vision for action processes. It is for that reason that after explicit learning performance is more easily compromised in the face of pressure or disorders. We present a way to deal with the issue of explicit learning during infancy.     

Toy-oriented changes in hand and joint kinematics during the emergence of purposeful reaching

Infants first consistently reach for objects between 3 and 5 months of age. In the months before reaching, infants produce a variety of arm movements. The relationship between these early arm movements and the emergence of purposeful reaching is still unclear. The purpose of the present study was to determine how groups of non-reaching, nearly reaching, and newly reaching infants changed the kinematics of their spontaneous arm movements in the presence of a toy. Five infants in each of these groups were observed with a high-speed motion capture system during trials with and without a toy present. Kinematic analyses examined 3D hand, shoulder, and elbow motions. Our results suggest that with a toy present, non-reachers altered their movement quantity whereas near- and new-reachers altered their movement quality through spatio-temporal dissociation and reorientation of the arm. When comparing the changes across groups we observed three preliminary patterns of toy-oriented changes. Our results join other studies to strengthen the relationship between early arm movements and purposeful reaching. Future longitudinal studies are now required to begin to fully understand the complex process by which infants adapt their early arm movements for purposeful behaviors.     

Getting the closer object? An information‐based dissociation between vision for perception and vision for movement in early infancy

In human adults two functionally and neuro‐anatomically separate systems exist for the use of visual information in perception and the use of visual information to control movements (Milner & Goodale, 1995 , 2008 ). We investigated whether this separation is already functioning in the early stages of the development of reaching. To this end, 6‐ and 7‐month‐old infants were presented with two identical objects at identical distances in front of an illusory Ponzo‐like background that made them appear to be located at different distances. In two further conditions without the illusory background, the two objects were presented at physically different distances. Preferential reaching outcomes indicated that the allocentric distance information contained in the illusory background affected the perception of object distance. Yet, infants' reaching kinematics were only affected by the objects' physical distance and not by the perceptual distance manipulation. These findings were taken as evidence for the two‐visual systems, as proposed by Milner and Goodale ( 2008 ), being functional in early infancy. We discuss the wider implications of this early dissociation.     

Proximodistal exploration in motor learning as an emergent property of optimization

To harness the complexity of their high‐dimensional bodies during sensorimotor development, infants are guided by patterns of freezing and freeing of degrees of freedom. For instance, when learning to reach, infants free the degrees of freedom in their arm proximodistally, that is, from joints that are closer to the body to those that are more distant. Here, we formulate and study computationally the hypothesis that such patterns can emerge spontaneously as the result of a family of stochastic optimization processes, without an innate encoding of a maturational schedule. In particular, we present simulated experiments with an arm where a computational learner progressively acquires reaching skills through adaptive exploration, and we show that a proximodistal organization appears spontaneously, which we denote PDFF (Proximo Distal Freezing and Freeing of degrees of freedom). We also compare this emergent organization between different arm morphologies—from human‐like to quite unnatural ones—to study the effect of different kinematic structures on the emergence of PDFF.     

Development of gaze aversion: Qualitative changes over the early school years

Looking away from an interlocutor's face during demanding cognitive activity can help adults and children answer challenging mental‐arithmetic and verbal‐reasoning questions ( Glenberg, Schroeder, & Robertson, 1998 ; Phelps, Doherty‐Sneddon, & Warnock, 2006 ). Whilst such ‘gaze aversion’ (GA) is used far less by 5‐year‐old schoolchildren, its use increases dramatically during the first years of primary education, reaching adult levels by 8 years of age ( Doherty‐Sneddon, Bruce, Bonner, Longbotham, & Doyle, 2002 ). The current study investigates whether developmental changes also occur in a qualitative aspect of GA – the direction of movement involved in GA shifts. Video data from eighteen 5‐year‐olds and nineteen 8‐year‐olds answering verbal and arithmetic questions were analysed for direction of GA. We found very different profiles of direction of GA across the two ages: whilst the 5‐year‐olds used predominantly rapid multidirectional ‘flicking’ movements and some sustained left lateral movements, the 8‐year‐olds used predominantly sustained rightward movements. It is concluded that there are concomitant qualitative changes in the nature of GA shifts as well as quantitative increases in the use of GA across these age groups. A model of human attention in face‐to‐face interaction is discussed, as are implications for the assessment of children's learning and development.     

Adults’ number-line estimation strategies: Evidence from eye movements

Although the development of number-line estimation ability is well documented, little is known of the processes underlying successful estimators’ mappings of numerical information onto spatial representations during these tasks. We tracked adults’ eye movements during a number-line estimation task to investigate the processes underlying number-to-space translation, with three main results. First, eye movements were strongly related to the target number’s location, and early processing measures directly predicted later estimation performance. Second, fixations and estimates were influenced by the size of the first number presented, indicating that adults calibrate their estimates online. Third, adults’ number-line estimates demonstrated patterns of error consistent with the predictions of psychophysical models of proportion estimation, and eye movement data predicted the specific error patterns we observed. These results support proportion-based accounts of number-line estimation and suggest that adults’ translation of numerical information into spatial representations is a rapid, online process.     

The development of rapid online control in children aged 6–12 years: Reaching performance

Rapid online control during reaching has an important bearing on movement accuracy and flexibility. It is surprising then that few studies have investigated the development of rapid online control in children. In this study, we were particularly interested in age-related changes in the nature of motor control in response to visual perturbation. We compared the performance of younger (6–7 years of age), mid-aged (8–9), and older (10–12) children, as well as healthy young adults using a double-step reaching task. Participants were required to make target-directed reaching movements in near space, while also responding to visual perturbations that occurred at movement onset for a small percentage of trials. Results showed that both the older and mid-aged children corrected their reaching in response to the unexpected shifts in target location significantly faster than younger children, manifest by reduced time to correction. In turn, the responses of adults were faster than older children in terms of movement time and on kinematic measures such as time to correction and time to peak velocity. These results indicate that the capacity to utilize forward estimates of limb position in the service of online control of early perturbations to ballistic (or rapid) reaching develops in a non-linear fashion, progressing rapidly between early and middle childhood, showing a degree of stability over mid and later childhood, but then evidence for continued refinement between childhood and young adulthood. The pattern of change after childhood and into early adolescence requires further investigation, particularly during the rapid phase of physical growth that accompanies puberty.     

Hierarchical Error Evaluation: The Role of Medial-Frontal Cortex in Postural Control

Motor error evaluation appears to be a hierarchically organized process subserved by 2 distinct systems: a higher level system within medial-frontal cortex responsible for movement outcome evaluation (high-level error evaluation) and a lower level posterior system(s) responsible for the mediation of within-movement errors (low-level error evaluation). While a growing body of evidence suggests that a reinforcement learning system within medial-frontal cortex plays a crucial role in the evaluation of high-level errors made during discrete reaching movements and continuous motor tracking, the role of this system in postural control is currently unclear. Participants learned a postural control task via a feedback-driven trial-and-error shaping process. In line with previous findings, electroencephalographic recordings revealed that feedback about movement outcomes elicited a feedback error–related negativity: a component of the human event-related brain potential associated with high-level outcome evaluation within medial-frontal cortex. Thus, the data provide evidence that a high-level error-evaluation system within medial-frontal cortex plays a key role in learning to control our body posture.     

Adults with probable developmental coordination disorder selectively process early visual,but not tactile information during action preparation. An electrophysiological study

Developmental coordination disorder (DCD) is a neurodevelopmental condition affecting motor coordination in children and adults. Here, EEG signals elicited by visual and tactile stimuli were recorded while adult participants with and without probable DCD (pDCD) performed a motor task. The task cued reaching movements towards a location in visible peripersonal space as well as an area of unseen personal space. Event-related potentials elicited by visual and tactile stimuli revealed that visual processing was strongly affected by movement preparation in the pDCD group, even more than in controls. However, in contrast to the controls, tactile processing in unseen space was unaffected by movement preparation in the pDCD group. The selective use of sensory information from vision and proprioception is fundamental for the adaptive control of movements, and these findings suggest that this is impaired in DCD. Additionally, the pDCD group showed attenuated motor rhythms (beta: 13–30 Hz) over sensorimotor regions following cues to prepare movements towards unseen personal space. The results reveal that individuals with pDCD exhibit differences in the neural mechanisms of spatial selection and action preparation compared to controls, which may underpin the sustained difficulties they experience. These findings provide new insights into the neural mechanisms potentially disrupted in this highly prevalent disorder.     

The Interaction of Body Morphology,Directional Kinematics,and Environmental Structure in the Generation of Neonatal Rat (Rattus norvegicus) Locomotor Behavior

We show that modeling directional kinematics is especially important for understanding spatial patterns of behavior in an arena. In rats, although patterns of locomotion appear to be under sensory control, they may be largely if not entirely explained, during early locomotor development, by the directional kinematics of random movement together with morphological/environmental constraints. Different relative probabilities of forward movement versus lateral movement (lateral:forward ratio; LFR) have dramatic consequences for the patterns of movement of modeled agents in an arena. These patterns of movement, produced by rigid-bodied agents, are also modified by increasing morphological realism in our model, wherein agents are able to bend and flex like rat pups. For both morphological designs, agents run with empirically derived LFRs matched metrics of movement for 7-day-old pups very well and 10-day-old rat pups fairly well. We conclude that LFR is an important parameter in modeling (a) patterns of dynamical behavior in an arena and (b) trajectories of behavioral development.     

Neuromuscular and spatial constraints on bimanual hand-held pendulum oscillations: dissociation or combination?

The present work investigated the effects of spatial and neuromuscular constraints on the mean states and variability of interlimb coordination patterns performed in the para-sagittal plane of motion in a hand-held pendulum oscillation task. Nine right-handed students had to oscillate two pendulums through wrist adduction-abduction movements. Relative movement direction was manipulated by asking participants to perform both isodirectional and non-isodirectional movements. Participants were required to grab the pendulums either with both forearms in the same neutral or supine posture or with one forearm in neutral while the other one was in prone-inversed position. When both forearms were in a similar posture, isodirectional movements were generated predominantly by simultaneous activation of homologous muscle groups whereas non-isodirectional movements mainly resulted from simultaneous activation of non-homologous muscle groups. When forearms were in dissimilar posture, isodirectional movements were generated predominantly by the simultaneous activation of non-homologous muscle groups whereas non-isodirectional movements mainly resulted from simultaneous activation of homologous muscle groups. Standard deviation of relative phase and absolute error of relative phase were analyzed for each forearm posture condition. We hypothesized that neuromuscular and spatial constraints would affect two different aspects of coordination performance, i.e., pattern stability and accuracy, respectively. Comparison of the results obtained for similar and dissimilar postures suggested that changes of pattern stability were mediated by changes in the nature of the muscle activation patterns that gave rise to wrist movement in each condition. On the other hand, the results also showed that movement direction exclusively affected phase shift. The findings are consistent with the conclusion of Park et al. [Park, H., Collins, D. R., & Turvey, M. T. (2001). Dissociation of muscular and spatial constraints on patterns of interlimb coordination. Journal of Experimental Psychology: Human Perception and Performance, 27, 32-47.] that neuromuscular constraints affect variability of relative phase (attractor strength) and spatial constraints affect the shift of relative phase (attractor location).     

Development of eye-movement control

Cognitive control of behavior continues to improve through adolescence in parallel with important brain maturational processes including synaptic pruning and myelination, which allow for efficient neuronal computations and the functional integration of widely distributed circuitries supporting top-down control of behavior. This is also a time when psychiatric disorders, such as schizophrenia and mood disorders, emerge reflecting a particularly vulnerability to impairments in development during adolescence. Oculomotor studies provide a unique neuroscientific approach to make precise associations between cognitive control and brain circuitry during development that can inform us of impaired systems in psychopathology. In this review, we first describe the development of pursuit, fixation, and visually-guided saccadic eye movements, which collectively indicate early maturation of basic sensorimotor processes supporting reflexive, exogenously-driven eye movements. We then describe the literature on the development of the cognitive control of eye movements as reflected in the ability to inhibit a prepotent eye movement in the antisaccade task, as well as making an eye movement guided by on-line spatial information in working memory in the oculomotor delayed response task. Results indicate that the ability to make eye movements in a voluntary fashion driven by endogenous plans shows a protracted development into adolescence. Characterizing the transition through adolescence to adult-level cognitive control of behavior can inform models aimed at understanding the neurodevelopmental basis of psychiatric disorders.     

The role of sensorimotor experience in the development of mimicry in infancy

During social interactions we often have an automatic and unconscious tendency to copy or ‘mimic’ others’ actions. The dominant view on the neural basis of mimicry appeals to an automatic coupling between perception and action. It has been suggested that this coupling is formed through associative learning during correlated sensorimotor experience. Although studies with adult participants have provided support for this hypothesis, little is known about the role of sensorimotor experience in supporting the development of perceptual‐motor couplings, and consequently mimicry behaviour, in infancy. Here we investigated whether the extent to which an observed action elicits mimicry depends on the opportunity an infant has had to develop perceptual‐motor couplings for this action through correlated sensorimotor experience. We found that mothers’ tendency to imitate their 4‐month‐olds’ facial expressions during a parent‐child interaction session was related to infants’ facial mimicry as measured by electromyography. Maternal facial imitation was not related to infants’ mimicry of hand actions, and instead we found preliminary evidence that infants’ tendency to look at their own hands may be related to their tendency to mimic hand actions. These results are consistent with the idea that mimicry is supported by perceptual‐motor couplings that are formed through correlated sensorimotor experience obtained by observing one's own actions and imitative social partners.     

Interpersonal synchrony increases prosocial behavior in infants

Adults who move together to a shared musical beat synchronously as opposed to asynchronously are subsequently more likely to display prosocial behaviors toward each other. The development of musical behaviors during infancy has been described previously, but the social implications of such behaviors in infancy have been little studied. In Experiment 1, each of 48 14‐month‐old infants was held by an assistant and gently bounced to music while facing the experimenter, who bounced either in‐synchrony or out‐of‐synchrony with the way the infant was bounced. The infants were then placed in a situation in which they had the opportunity to help the experimenter by handing objects to her that she had ‘accidently’ dropped. We found that 14‐month‐old infants were more likely to engage in altruistic behavior and help the experimenter after having been bounced to music in synchrony with her, compared to infants who were bounced to music asynchronously with her. The results of Experiment 2, using anti‐phase bouncing, suggest that this is due to the contingency of the synchronous movements as opposed to movement symmetry. These findings support the hypothesis that interpersonal motor synchrony might be one key component of musical engagement that encourages social bonds among group members, and suggest that this motor synchrony to music may promote the very early development of altruistic behavior. A video abstract of this article can be viewed at http://www.youtube.com/watch?v=IaqWehfDm7c&feature=youtu.be