Development of multisensory reweighting is impaired for quiet stance control in children with developmental coordination disorder (DCD)

Background

Developmental Coordination Disorder (DCD) is a leading movement disorder in children that commonly involves poor postural control. Multisensory integration deficit, especially the inability to adaptively reweight to changing sensory conditions, has been proposed as a possible mechanism but with insufficient characterization. Empirical quantification of reweighting significantly advances our understanding of its developmental onset and improves the characterization of its difference in children with DCD compared to their typically developing (TD) peers.

Methodology/Principal Findings

Twenty children with DCD (6.6 to 11.8 years) were tested with a protocol in which visual scene and touch bar simultaneously oscillateded medio-laterally at different frequencies and various amplitudes. Their data were compared to data on TD children (4.2 to 10.8 years) from a previous study. Gains and phases were calculated for medio-lateral responses of the head and center of mass to both sensory stimuli. Gains and phases were simultaneously fitted by linear functions of age for each amplitude condition, segment, modality and group. Fitted gains and phases at two comparison ages (6.6 and 10.8 years) were tested for reweighting within each group and for group differences. Children with DCD reweight touch and vision at a later age (10.8 years) than their TD peers (4.2 years). Children with DCD demonstrate a weak visual reweighting, no advanced multisensory fusion and phase lags larger than those of TD children in response to both touch and vision.

Conclusions/Significance

Two developmental perspectives, postural body scheme and dorsal stream development, are provided to explain the weak vision reweighting. The lack of multisensory fusion supports the notion that optimal multisensory integration is a slow developmental process and is vulnerable in children with DCD.     

Children and Older Adults Exhibit Distinct Sub-Optimal Cost-Benefit Functions when Preparing to Move Their Eyes and Hands

Numerous activities require an individual to respond quickly to the correct stimulus. The provision of advance information allows response priming but heightened responses can cause errors (responding too early or reacting to the wrong stimulus). Thus, a balance is required between the online cognitive mechanisms (inhibitory and anticipatory) used to prepare and execute a motor response at the appropriate time. We investigated the use of advance information in 71 participants across four different age groups: (i) children, (ii) young adults, (iii) middle-aged adults, and (iv) older adults. We implemented ‘cued’ and ‘non-cued’ conditions to assess age-related changes in saccadic and touch responses to targets in three movement conditions: (a) Eyes only; (b) Hands only; (c) Eyes and Hand. Children made less saccade errors compared to young adults, but they also exhibited longer response times in cued versus non-cued conditions. In contrast, older adults showed faster responses in cued conditions but exhibited more errors. The results indicate that young adults (18–25 years) achieve an optimal balance between anticipation and execution. In contrast, children show benefits (few errors) and costs (slow responses) of good inhibition when preparing a motor response based on advance information; whilst older adults show the benefits and costs associated with a prospective response strategy (i.e., good anticipation).     

A competitive integration model of exogenous and endogenous eye movements

We present a model of the eye movement system in which the programming of an eye movement is the result of the competitive integration of information in the superior colliculi (SC). This brain area receives input from occipital cortex, the frontal eye fields, and the dorsolateral prefrontal cortex, on the basis of which it computes the location of the next saccadic target. Two critical assumptions in the model are that cortical inputs are not only excitatory, but can also inhibit saccades to specific locations, and that the SC continue to influence the trajectory of a saccade while it is being executed. With these assumptions, we account for many neurophysiological and behavioral findings from eye movement research. Interactions within the saccade map are shown to account for effects of distractors on saccadic reaction time (SRT) and saccade trajectory, including the global effect and oculomotor capture. In addition, the model accounts for express saccades, the gap effect, saccadic reaction times for antisaccades, and recorded responses from neurons in the SC and frontal eye fields in these tasks.     

A Mathematical Model of Optimal Saccadic Eye Movement by a Pair of Muscles

This paper presents a model of saccadic eye movements. Eye movements are considered as being ballistic, since saccades (rapid concurrent movements of both eyes) occur several hundred thousand times per day; visual perception of the environment is interrupted by a saccade. The optimal control was constructed for the motion considered in three consecutively refined assumptions. The controls included in the time-optimal problem were the resultant moment of force exerted by the extraocular muscles, individual moments of force exerted by either muscle of the agonist–antagonist pair, and finally, the rate of change of these moments. This approach is consistent with the view that is currently upheld by physiologists, who believe that a saccade is programmed by the central nervous system before the beginning of an eye movement and is scarcely adjusted during the movement itself. The solution of the optimal control problem and the results obtained by subsequent numerical modeling of saccadic trajectories were compared with the published experimental data. The saccadic trajectories were compared based on the main sequence, the known consistent relationship between saccade amplitude and duration, which is the most widely applied and commonly accepted way of describing saccade data. The main sequence of saccades obtained from the solution of the optimal control problem formulated in the most complete form agreed well with published experimental results.     

Sensory processing of motor inaccuracy depends on previously performed movement and on subsequent motor corrections: a study of the saccadic system

When goal-directed movements are inaccurate, two responses are generated by the brain: a fast motor correction toward the target and an adaptive motor recalibration developing progressively across subsequent trials. For the saccadic system, there is a clear dissociation between the fast motor correction (corrective saccade production) and the adaptive motor recalibration (primary saccade modification). Error signals used to trigger corrective saccades and to induce adaptation are based on post-saccadic visual feedback. The goal of this study was to determine if similar or different error signals are involved in saccadic adaptation and in corrective saccade generation. Saccadic accuracy was experimentally altered by systematically displacing the visual target during motor execution. Post-saccadic error signals were studied by manipulating visual information in two ways. First, the duration of the displaced target after primary saccade termination was set at 15, 50, 100 or 800 ms in different adaptation sessions. Second, in some sessions, the displaced target was followed by a visual mask that interfered with visual processing. Because they rely on different mechanisms, the adaptation of reactive saccades and the adaptation of voluntary saccades were both evaluated. We found that saccadic adaptation and corrective saccade production were both affected by the manipulations of post-saccadic visual information, but in different ways. This first finding suggests that different types of error signal processing are involved in the induction of these two motor corrections. Interestingly, voluntary saccades required a longer duration of post-saccadic target presentation to reach the same amount of adaptation as reactive saccades. Finally, the visual mask interfered with the production of corrective saccades only during the voluntary saccades adaptation task. These last observations suggest that post-saccadic perception depends on the previously performed action and that the differences between saccade categories of motor correction and adaptation occur at an early level of visual processing.     

Saccadic head movements of the praying mantis, with particular reference to visual and proprioceptive information

ABSTRACT. Horizontal head movements of the praying mantis, Sphodromantis lineola Burm., were recorded continuously. They responded to the presence of a live blowfly prey in the antero-lateral visual field with a rapid saccadic head movement. The angular movement of a fixation saccade was correlated positively to the displacement of the prey from the prothoracic midline. Saccade magnitude and velocity are related. After the stimulus moved out of the visual field, the mantis made a second saccadic head movement, a return saccade towards the body midline. We observed return saccades in which the head overshot or undershot the body midline, as well as saccades which returned the head exactly to its initial position. In 92% of trials with intact mantids, the return movement succeeded eventually in rotating the head back to its initial position, whereas after removal of the neck hair plates this occurred in only 47% of trials. There is a consistent relation between saccade extent and velocity. Velocities of return saccades were slower than those of fixation saccades. It is suggested that sensory inputs from the neck hair plate proprioceptors modify both the magnitude and the angular velocity of fixation and return saccadic head movements.     

Effect of dopamine deficiency on the preparation of visually guided saccadic eye movements

Parameters of saccadic eye movements were studied in patients with Parkinson's disease and control subjects. In parkinsonian patients, the number of slow regular saccades was shown to be increased, and the number of express saccades was shown to be decreased. As a result the mean of saccade latency in patients was longer than in the control group. Moreover, the percentage of multistep saccades in patients with Parkinson's disease. In this case, not one but two or three saccades were performed with smaller amplitude to the target. We point, that the multistep saccades occurred mainly among the express saccades. Obviously, the dopamine deficiency distinguishing parkinsonian patients takes the primary part in the development of saccadic disorders. Degeneration of the nigrostriatal dopamine pathway results in imbalance in activity of the direct and indirect output pathways of the striatum. We suppose that this leads to inhibition of neurons activity in the superior colliculus during the saccade performance, which results in the early saccade interruption. In support of this reasoning, the mean of saccade latency and the percentage of the multistep saccades decreased in patients with Parkinson's disease after dopamine D2/D3 agonist (piribedil) treatment, due to activity restoration of the indirect pathway.     

Both Lexical and Non-Lexical Characters Are Processed during Saccadic Eye Movements

On average our eyes make 3–5 saccadic movements per second when we read, although their neural mechanism is still unclear. It is generally thought that saccades help redirect the retinal fovea to specific characters and words but that actual discrimination of information only occurs during periods of fixation. Indeed, it has been proposed that there is active and selective suppression of information processing during saccades to avoid experience of blurring due to the high-speed movement. Here, using a paradigm where a string of either lexical (Chinese) or non-lexical (alphabetic) characters are triggered by saccadic eye movements, we show that subjects can discriminate both while making saccadic eye movement. Moreover, discrimination accuracy is significantly better for characters scanned during the saccadic movement to a fixation point than those not scanned beyond it. Our results showed that character information can be processed during the saccade, therefore saccades during reading not only function to redirect the fovea to fixate the next character or word but allow pre-processing of information from the ones adjacent to the fixation locations to help target the next most salient one. In this way saccades can not only promote continuity in reading words but also actively facilitate reading comprehension.     

Motor Learning: An Analysis of 100 Trials of a Ski Slalom Game in Children with and without Developmental Coordination Disorder

ObjectiveAlthough Developmental Coordination Disorder (DCD) is often characterized as a skill acquisition deficit disorder, few studies have addressed the process of motor learning. This study examined learning of a novel motor task; the Wii Fit ski slalom game. The main objectives were to determine: 1) whether learning occurs over 100 trial runs of the game, 2) if the learning curve is different between children with and without DCD, 3) if learning is different in an easier or harder version of the task, 4) if learning transfers to other balance tasks.Method17 children with DCD (6–10 years) and a matched control group of 17 typically developing (TD) children engaged in 20 minutes of gaming, twice a week for five weeks. Each training session comprised of alternating trial runs, with five runs at an easy level and five runs at a difficult level. Wii scores, which combine speed and accuracy per run, were recorded. Standardized balance tasks were used to measure transfer.ResultsSignificant differences in initial performance were found between groups on the Wii score and balance tasks. Both groups improved their Wii score over the five weeks. Improvement in the easy and in the hard task did not differ between groups. Retention in the time between training sessions was not different between TD and DCD groups either. The DCD group improved significantly on all balance tasks.ConclusionsThe findings in this study give a fairly coherent picture of the learning process over a medium time scale (5 weeks) in children novice to active computer games; they learn, retain and there is evidence of transfer to other balance tasks. The rate of motor learning is similar for those with and without DCD. Our results raise a number of questions about motor learning that need to be addressed in future research.     

Eye movements modulate visual receptive fields of V4 neurons

The receptive field, defined as the spatiotemporal selectivity of neurons to sensory stimuli, is central to our understanding of the neuronal mechanisms of perception. However, despite the fact that eye movements are critical during normal vision, the influence of eye movements on the structure of receptive fields has never been characterized. Here, we map the receptive fields of macaque area V4 neurons during saccadic eye movements and find that receptive fields are remarkably dynamic. Specifically, before the initiation of a saccadic eye movement, receptive fields shrink and shift towards the saccade target. These spatiotemporal dynamics may enhance information processing of relevant stimuli during the scanning of a visual scene, thereby assisting the selection of saccade targets and accelerating the analysis of the visual scene during free viewing.     

The Fixation and Saccade P3

Although most instances of object recognition during natural viewing occur in the presence of saccades, the neural correlates of objection recognition have almost exclusively been examined during fixation. Recent studies have indicated that there are post-saccadic modulations of neural activity immediately following eye movement landing; however, whether post-saccadic modulations affect relatively late occurring cognitive components such as the P3 has not been explored. The P3 as conventionally measured at fixation is commonly used in brain computer interfaces, hence characterizing the post-saccadic P3 could aid in the development of improved brain computer interfaces that allow for eye movements. In this study, the P3 observed after saccadic landing was compared to the P3 measured at fixation. No significant differences in P3 start time, temporal persistence, or amplitude were found between fixation and saccade trials. Importantly, sensory neural responses canceled in the target minus distracter comparisons used to identify the P3. Our results indicate that relatively late occurring cognitive neural components such as the P3 are likely less sensitive to post saccadic modulations than sensory neural components and other neural activity occurring shortly after eye movement landing. Furthermore, due to the similarity of the fixation and saccade P3, we conclude that the P3 following saccadic landing could possibly be used as a viable signal in brain computer interfaces allowing for eye movements.     

Response Inhibition Impairment in High Functioning Autism and Attention Deficit Hyperactivity Disorder: Evidence from Near-Infrared Spectroscopy Data

Background

Response inhibition, an important domain of executive function (EF), involves the ability to suppress irrelevant or interfering information and impulses. Previous studies have shown impairment of response inhibition in high functioning autism (HFA) and attention deficit hyperactivity disorder (ADHD), but more recent findings have been inconsistent. To date, almost no studies have been conducted using functional imaging techniques to directly compare inhibitory control between children with HFA and those with ADHD.

Method

Nineteen children with HFA, 16 age- and intelligence quotient (IQ)-matched children with ADHD, and 16 typically developing (TD) children were imaged using functional near-infrared spectroscopy (NIRS) while performing Go/No-go and Stroop tasks.

Results

Compared with the TD group, children in both the HFA and ADHD groups took more time to respond during the No-go blocks, with reaction time longest for HFA and shortest for TD. Children in the HFA and ADHD groups also made a greater number of reaction errors in the No-go blocks than those in the TD group. During the Stroop task, there were no significant differences between these three groups in reaction time and omission errors. Both the HFA and ADHD groups showed a higher level of inactivation in the right prefrontal cortex (PFC) during the No-go blocks, relative to the TD group. However, no significant differences were found between groups in the levels of oxyhemoglobin concentration in the PFC during the Stroop task.

Conclusion

Functional brain imaging using NIRS showed reduced activation in the right PFC in children with HFA or ADHD during an inhibition task, indicating that inhibitory dysfunction is a shared feature of both HFA and ADHD.     

Saccadic adaptation to moving targets

Saccades are so called ballistic movements which are executed without online visual feedback. After each saccade the saccadic motor plan is modified in response to post-saccadic feedback with the mechanism of saccadic adaptation. The post-saccadic feedback is provided by the retinal position of the target after the saccade. If the target moves after the saccade, gaze may follow the moving target. In that case, the eyes are controlled by the pursuit system, a system that controls smooth eye movements. Although these two systems have in the past been considered as mostly independent, recent lines of research point towards many interactions between them. We were interested in the question if saccade amplitude adaptation is induced when the target moves smoothly after the saccade. Prior studies of saccadic adaptation have considered intra-saccadic target steps as learning signals. In the present study, the intra-saccadic target step of the McLaughlin paradigm of saccadic adaptation was replaced by target movement, and a post-saccadic pursuit of the target. We found that saccadic adaptation occurred in this situation, a further indication of an interaction of the saccadic system and the pursuit system with the aim of optimized eye movements.     

Human fast negative EEG potentials before express saccades

Fast negative EEG potentials preceding fast regular saccades and express saccades were studied by the method of backward averaging under conditions of monocular stimulation of the right and left eye. "Step" and "gap" experimental paradigms were used for visual stimulation. Analysis of parameters of potentials and their spatiotemporal dynamics suggests that, under conditions of the increased attention and optimal readiness of the neural structures, express saccades appear when the previously chosen program of the future eye movement coincides with the actual target coordinates. We assumed that the saccade latency decreases at the expense of the involvement of the main oculomotor areas of motor and saccadic planning in its initiation; an express saccade can be initiated also by means of direct transmission of the signal from the cortex to the brainstem saccadic generator passing by the superior colliculus. Moreover, anticipating release from the central fixation and attention distraction are necessary for the successful initiation of an express saccade.     

How Do I Fit through That Gap? Navigation through Apertures in Adults with and without Developmental Coordination Disorder

During everyday life we move around busy environments and encounter a range of obstacles, such as a narrow aperture forcing us to rotate our shoulders in order to pass through. In typically developing individuals the decision to rotate the shoulders is body scaled and this movement adaptation is temporally and spatially tailored to the size of the aperture. This is done effortlessly although it actually involves many complex skills. For individuals with Developmental Coordination Disorder (DCD) moving in a busy environment and negotiating obstacles presents a real challenge which can negatively impact on safety and participation in motor activities in everyday life. However, we have a limited understanding of the nature of the difficulties encountered. Therefore, this current study considered how adults with DCD make action judgements and movement adaptations while navigating apertures. Fifteen adults with DCD and 15 typically developing (TD) controls passed through a series of aperture sizes which were scaled to body size (0.9-2.1 times shoulder width). Spatial and temporal characteristics of movement were collected over the approach phase and while crossing the aperture. The decision to rotate the shoulders was not scaled in the same way for the two groups, with the adults with DCD showing a greater propensity to turn for larger apertures compared to the TD adults when body size alone was accounted for. However, when accounting for degree of lateral trunk movement and variability on the approach, we no longer saw differences between the two groups. In terms of the movement adaptations, the adults with DCD approached an aperture differently when a shoulder rotation was required and then adapted their movement sooner compared to their typical peers. These results point towards an adaptive strategy in adults with DCD which allows them to account for their movement difficulties and avoid collision.     

Gap Effect Abnormalities during a Visually Guided Pro-Saccade Task in Children with Attention Deficit Hyperactivity Disorder

Attention deficit hyperactivity disorder (ADHD) is a neurodevelopmental disorder that starts in early childhood and has a comprehensive impact on psychosocial activity and education as well as general health across the lifespan. Despite its prevalence, the current diagnostic criteria for ADHD are debated. Saccadic eye movements are easy to quantify and may be a quantitative biomarker for a wide variety of neurological and psychiatric disorders, including ADHD. The goal of this study was to examine whether children with ADHD exhibit abnormalities during a visually guided pro-saccadic eye-movement and to clarify the neurophysiological mechanisms associated with their behavioral impairments. Thirty-seven children with ADHD (aged 5–11 years) and 88 typically developing (TD) children (aged 5–11 years) were asked to perform a simple saccadic eye-movement task in which step and gap conditions were randomly interleaved. We evaluated the gap effect, which is the difference in the reaction time between the two conditions. Children with ADHD had a significantly longer reaction time than TD children (p < 0.01) and the gap effect was markedly attenuated (p < 0.01). These results suggest that the measurement of saccadic eye movements may provide a novel method for evaluating the behavioral symptoms and clinical features of ADHD, and that the gap effect is a potential biomarker for the diagnosis of ADHD in early childhood.     

Figure-ground activity in V1 and guidance of saccadic eye movements.

Every day we shift our gaze about 150.000 times mostly without noticing it. The direction of these gaze shifts are not random but directed by sensory information and internal factors. After each movement the eyes hold still for a brief moment so that visual information at the center of our gaze can be processed in detail. This means that visual information at the saccade target location is sufficient to accurately guide the gaze shift but yet is not sufficiently processed to be fully perceived. In this paper I will discuss the possible role of activity in the primary visual cortex (V1), in particular figure-ground activity, in oculo-motor behavior. Figure-ground activity occurs during the late response period of V1 neurons and correlates with perception. The strength of figure-ground responses predicts the direction and moment of saccadic eye movements. The superior colliculus, a gaze control center that integrates visual and motor signals, receives direct anatomical connections from V1. These projections may convey the perceptual information that is required for appropriate gaze shifts. In conclusion, figure-ground activity in V1 may act as an intermediate component linking visual and motor signals.     

Saccadic Momentum and Facilitation of Return Saccades Contribute to an Optimal Foraging Strategy

The interest in saccadic IOR is funneled by the hypothesis that it serves a clear functional purpose in the selection of fixation points: the facilitation of foraging. In this study, we arrive at a different interpretation of saccadic IOR. First, we find that return saccades are performed much more often than expected from the statistical properties of saccades and saccade pairs. Second, we find that fixation durations before a saccade are modulated by the relative angle of the saccade, but return saccades show no sign of an additional temporal inhibition. Thus, we do not find temporal saccadic inhibition of return. Interestingly, we find that return locations are more salient, according to empirically measured saliency (locations that are fixated by many observers) as well as stimulus dependent saliency (defined by image features), than regular fixation locations. These results and the finding that return saccades increase the match of individual trajectories with a grand total priority map evidences the return saccades being part of a fixation selection strategy that trades off exploration and exploitation.     

Investigation of saccadic eye movement effects on the fluid dynamic in the anterior chamber

The aqueous humor (AH) flow in the anterior chamber (AC) due to saccadic movements is investigated in this research. The continuity, Navier-Stokes and energy equations in 3D and unsteady forms are solved numerically and the saccadic motion was modeled by the dynamic mesh technique. Firstly, the numerical model was validated for the saccadic movement of a spherical cavity with analytic solutions and experimental data where excellent agreement was observed. Then, two types of periodic and realistic saccadic motions of the AC are simulated, whereby the flow field is computed for various saccade amplitudes and the results are reported for different times. The results show that the acting shear stress on the corneal endothelial cells from AH due to saccadic movements is much higher than that due to normal AH flow by buoyancy induced due to temperature gradient. This shear stress is higher on the central region of the cornea. The results also depict that eye saccade imposes a 3D complicated flow field in the AC consist of various vortex structures. Finally, the enchantment of heat transfer in the AC by AH mixing as a result of saccadic motion is investigated.     

Eye-Hand Synergy and Intermittent Behaviors during Target-Directed Tracking with Visual and Non-visual Information

Visual feedback and non-visual information play different roles in tracking of an external target. This study explored the respective roles of the visual and non-visual information in eleven healthy volunteers who coupled the manual cursor to a rhythmically moving target of 0.5 Hz under three sensorimotor conditions: eye-alone tracking (EA), eye-hand tracking with visual feedback of manual outputs (EH tracking), and the same tracking without such feedback (EHM tracking). Tracking error, kinematic variables, and movement intermittency (saccade and speed pulse) were contrasted among tracking conditions. The results showed that EHM tracking exhibited larger pursuit gain, less tracking error, and less movement intermittency for the ocular plant than EA tracking. With the vision of manual cursor, EH tracking achieved superior tracking congruency of the ocular and manual effectors with smaller movement intermittency than EHM tracking, except that the rate precision of manual action was similar for both types of tracking. The present study demonstrated that visibility of manual consequences altered mutual relationships between movement intermittency and tracking error. The speed pulse metrics of manual output were linked to ocular tracking error, and saccade events were time-locked to the positional error of manual tracking during EH tracking. In conclusion, peripheral non-visual information is critical to smooth pursuit characteristics and rate control of rhythmic manual tracking. Visual information adds to eye-hand synchrony, underlying improved amplitude control and elaborate error interpretation during oculo-manual tracking.