A review of five tests to identify motor coordination difficulties in young adults

Difficulties with low motor competence in childhood and adolescence, such as that seen in Developmental Coordination Disorder (DCD), often persist into adulthood. Identification of DCD at all ages is particularly challenging and problematic because of the diversity of motor symptoms. Many tests of motor proficiency and impairment have been developed for children up to 12 years of age. Whilst identification of DCD is important during childhood, it is of equal importance to identify and monitor the impact of this impairment as an individual grows and develops. Currently there is no test specifically designed to support diagnosis and monitor change in the age range 16–30 years. In this article we review five tests that have been used to assess motor competence among young adults (Bruininks–Oseretsky Test of Motor Proficiency-2, McCarron Assessment of Neuromuscular Development, Movement Assessment Battery for Children-2, Tufts Assessment of Motor Performance and the Zurich Neuromotor Assessment). Key issues relevant to testing motor skills in older populations, such as the inclusion of age appropriate skills, are explored. While the BOT-2 provided the most evidence for valid and reliable measurement of Criterion A of the diagnostic criteria for DCD among this age group, no test adequately evaluated Criterion B. Further evaluation of motor skill assessment among the young adult population is needed.     

Parallel contributions of cerebellar, striatal and M1 mechanisms to motor sequence learning

When learning a new motor sequence, we must execute the correct order of movements while simultaneously optimizing sensorimotor parameters such as trajectory, timing, velocity and force. Neurophysiological studies in animals and humans have identified the major brain regions involved in sequence learning, including the motor cortex (M1), basal ganglia (BG) and cerebellum. Current models link these regions to different stages of learning (early vs. late) or different components of performance (spatial vs. sensorimotor). At the same time, research in motor control has given rise to the concept that internal models at different levels of the motor system may contribute to learning. The goal of this review is to develop a new framework for motor sequence learning that combines stage and component models within the context of internal models. To do this, we review behavioral and neuroimaging studies in humans and neurophysiological studies in animals. Based on this evidence, we present a model proposing that sequence learning is underwritten by parallel, interacting processes, including internal model formation and sequence representation, that are instantiated in specific cerebellar, BG or M1 mechanisms depending on task demands and the stage of learning. The striatal system learns predictive stimulus-response associations and is critical for motor chunking. The role of the cerebellum is to acquire the optimal internal model for sequence performance in a particular context, and to contribute to error correction and control of on-going movement. M1 acts to store the representation of a learned sequence, likely as part of a distributed network including the parietal lobe and premotor cortex.     

Intact procedural motor sequence learning in developmental coordination disorder

The purpose of the present study was to explore the possibility of a procedural learning deficit among children with developmental coordination disorder (DCD). We tested 34 children aged 6–12 years with and without DCD using the serial reaction time task, in which the standard keyboard was replaced by a touch screen in order to minimize the impact of perceptuomotor coordination difficulties that characterize this disorder. The results showed that children with DCD succeed as well as control children at the procedural sequence learning task. These findings challenge the hypothesis that a procedural learning impairment underlies the difficulties of DCD children in acquiring and automatizing daily activities. We suggest that the previously reported impairment of children with DCD on the serial reaction time task is not due to a sequence learning deficit per se, but rather due to methodological factors such as the response mode used in these studies.     

Compromised motor control in children with DCD: A deficit in the internal model?—A systematic review

A viable hypothesis to explain the compromised motor ability of children with Developmental Coordination Disorder (DCD) suggests a fundamental deficit in their ability to utilize internal models for motor control. Dysfunction in this mode of control is thought to compromise their motor learning capabilities. The aim of this systematic review is to examine the available evidence for the internal modeling deficit (IMD) hypothesis. A systematic review using five databases identified 48 relevant articles. These studies were categorized according to the effector system involved in the evaluation of motor control and were evaluated for methodological quality. In most papers, DSM-IV-TR criteria for the classification of DCD were not completely fulfilled and possible attentional problems not accounted for. Results showed compromised control of overt and covert eye movements, dynamic postural control, manual control for tasks that vary in complexity, and for motor imagery of manual and whole-body postures. Importantly, this review shows support for general hypothesis that deficits of predictive control manifest in DCD across effector systems.     

Do children with autism spectrum disorders have motor learning difficulties?

Autism spectrum disorder (ASD) is a neurodevelopmental disorder characterized by social and communication impairments as well as a wide range of behavioral symptoms. For years, motor disturbance reported in ASD has not been treated as a core deficit because of the overwhelming problems in sociability and communication. Recent studies, however, reveal that motor deficits are also fundamental to ASD presentation and contribute to the core symptoms of ASD. Untreated motor problems can persist well into adolescence and adulthood, resulting in long-term physical, psychological, and behavioral issues in individuals with ASD. Thus, the ability to understand and address the overall picture of a child with ASD, including motor dysfunction, has become a critical need. This review focuses on sensorimotor adaptation and motor sequence learning in children with ASD and presents related evidence that compromised motor learning may play a critical role in motor dysfunctions of ASD. It addresses possible factors that explain controversial findings in the literature and discusses potential strategies for facilitating motor learning. Future intervention studies should address the importance of motor learning beyond social and language domains in ASD.     

Impaired visuo-motor sequence learning in Developmental Coordination Disorder

The defining feature of Developmental Coordination Disorder (DCD) is the marked impairment in the development of motor coordination (DSM-IV-TR, American Psychiatric Association, 2000). In the current study, we focused on one core aspect of motor coordination: learning to correctly sequence movements. We investigated the procedural, visuo-motor sequence learning abilities of 18 children with DCD and 20 matched typically developing (TD) children, by means of the serial reaction time (SRT) task. Reaction time measurements yielded two important findings. Overall, DCD children demonstrated general learning of visuo-motor task demands comparable to that of TD children but failed to learn the visuo-motor sequence. Interestingly, a sequence recall test, administered after the SRT task, indicated some awareness of the repeating sequence pattern. This suggests that the sequence learning problems of DCD children might be located at the stage of motor planning rather than sequence acquisition.     

Unique deficit in embodied simulation in autism: An fMRI study comparing autism and developmental coordination disorder

A deficit in pre‐cognitively mirroring other people''s actions and experiences may be related to the social impairments observed in autism spectrum disorder (ASD). However, it is unclear whether such embodied simulation deficits are unique to ASD or instead are related to motor impairment, which is commonly comorbid with ASD. Here we aim to disentangle how, neurologically, motor impairments contribute to simulation deficits and identify unique neural signatures of ASD. We compare children with ASD (N = 30) to children with Developmental Coordination Disorder (DCD; N = 23) as well as a typically developing group (N = 33) during fMRI tasks in which children observe, imitate, and mentalize about other people''s actions. Results indicate a unique neural signature in ASD: during action observation, only the ASD group shows hypoactivity in a region important for simulation (inferior frontal gyrus, pars opercularis, IFGop). However, during a motor production task (imitation), the IFGop is hypoactive for both ASD and DCD groups. For all tasks, we find correlations across groups with motor ability, even after controlling for age, IQ, and social impairment. Conversely, across groups, mentalizing ability is correlated with activity in the dorsomedial prefrontal cortex when controlling for motor ability. These findings help identify the unique neurobiological basis of ASD for aspects of social processing. Furthermore, as no previous fMRI studies correlated brain activity with motor impairment in ASD, these findings help explain prior conflicting reports in these simulation networks.     

A systematic review of mirror neuron system function in developmental coordination disorder: Imitation,motor imagery,and neuroimaging evidence

PURPOSEThe aim of this systematic review was to investigate the evidence of abnormal functioning of the mirror neuron system (MNS) in children and adults with developmental coordination disorder (DCD), through examination of imitation, motor imagery, and neuroimaging literature.METHODSThe following databases were comprehensively searched for relevant articles: CINAHL Plus, Embase, MEDLINE, PsycINFO, Pubmed, and Web of Science. Full-text articles of all potentially relevant citations were obtained and assessed for eligibility by two authors. Outcome measures of interest at a motor behaviour level were any measures of imitation or motor imagery proficiency and, at a neurological level, were any measures of neural activity in MNS brain regions. Due to differences in outcome measures between studies and the variables reported, a narrative review was undertaken to synthesise findings from the studies.RESULTSOverall, 31 articles met the inclusion criteria. Children and adults with DCD display deficits imitating meaningful and novel gestures and demonstrate different response patterns to controls when undertaking complex motor imagery tasks. Children with DCD present reduced activation and connectivity of frontal, parietal, and temporal MNS regions.CONCLUSIONSPreliminary evidence indicates some deficit in the functioning of the MNS at a motor behaviour and neurological level. As no published neuroimaging studies have been designed specifically to explore MNS function, these results must be interpreted with caution. Further research to explore the MNS hypothesis in greater detail, particularly from a neuroimaging perspective, has the potential to provide information on the underlying mechanisms of DCD, inform future research into the aetiology of this disorder, and inform intervention approaches.     

The cholinergic system and Parkinson disease

Although Parkinson disease (PD) is viewed traditionally as a motor syndrome secondary to nigrostriatal dopaminergic denervation, recent studies emphasize non-motor features. Non-motor comorbidities, such as cognitive impairment, are likely the result of an intricate interplay of multi-system degenerations and neurotransmitter deficiencies extending beyond the loss of dopaminergic nigral neurons. The pathological hallmark of parkinsonian dementia is the presence of extra-nigral Lewy bodies that can be accompanied by other pathologies, such as senile plaques. Lewy first identified the eponymous Lewy body in neurons of the nucleus basalis of Meynert (nbM), the source of cholinergic innervation of the cerebral cortex. Although cholinergic denervation is recognized as a pathological hallmark of Alzheimer disease (AD), in vivo neuroimaging studies reveal loss of cerebral cholinergic markers in parkinsonian dementia similar to or more severe than in prototypical AD. Imaging studies agree with post-mortem evidence suggesting that basal forebrain cholinergic system degeneration appears early in PD and worsens coincident with the appearance of dementia. Early cholinergic denervation in PD without dementia appears to be heterogeneous and may make specific contributions to the PD clinical phenotype. Apart from well-known cognitive and behavioral deficits, central, in particular limbic, cholinergic denervation may be associated with progressive deficits of odor identification in PD. Recent evidence indicates also that subcortical cholinergic denervation, probably due to degeneration of brainstem pedunculopontine nucleus neurons, may relate to the presence of dopamine non-responsive gait and balance impairments, including falls, in PD.     

Motor learning requires myelination to reduce asynchrony and spontaneity in neural activity

Myelination increases the conduction velocity in long-range axons and is prerequisite for many brain functions. Impaired myelin regulation or impairment of myelin itself is frequently associated with deficits in learning and cognition in neurological and psychiatric disorders. However, it has not been revealed what perturbation of neural activity induced by myelin impairment causes learning deficits. Here, we measured neural activity in the motor cortex during motor learning in transgenic mice with a subtle impairment of their myelin. This deficit in myelin impaired motor learning, and was accompanied by a decrease in the amplitude of movement-related activity and an increase in the frequency of spontaneous activity. Thalamocortical axons showed variability in axonal conduction with a large spread in the timing of postsynaptic cortical responses. Repetitive pairing of forelimb movements with optogenetic stimulation of thalamocortical axon terminals restored motor learning. Thus, myelin regulation helps to maintain the synchrony of cortical spike-time arrivals through long-range axons, facilitating the propagation of the information required for learning. Our results revealed the pathological neuronal circuit activity with impaired myelin and suggest the possibility that pairing of noninvasive brain stimulation with relevant behaviors may ameliorate cognitive and behavioral abnormalities in diseases with impaired myelination.     

Toward a motor signature in autism: Studies from human-machine interaction

BackgroundAutism spectrum disorder (ASD) is a heterogeneous group of neurodevelopmental disorders which core symptoms are impairments in socio-communication and repetitive symptoms and stereotypies. Although not cardinal symptoms per se, motor impairments are fundamental aspects of ASD. These impairments are associated with postural and motor control disabilities that we investigated using computational modeling and developmental robotics through human-machine interaction paradigms.MethodFirst, in a set of studies involving a human–robot posture imitation, we explored the impact of 3 different groups of partners (including a group of children with ASD) on robot learning by imitation. Second, using an ecological task, i.e. a real-time motor imitation with a tightrope walker (TW) avatar, we investigated interpersonal synchronization, motor coordination and motor control during the task in children with ASD (n = 29), TD children (n = 39) and children with developmental coordination disorder (n = 17, DCD).ResultsFrom the human–robot experiments, we evidenced that motor signature at both groups’ and individuals’ levels had a key influence on imitation learning, posture recognition and identity recognition. From the more dynamic motor imitation paradigm with a TW avatar, we found that interpersonal synchronization, motor coordination and motor control were more impaired in children with ASD compared to both TD children and children with DCD. Taken together these results confirm the motor peculiarities of children with ASD despite imitation tasks were adequately performed.DiscussionStudies from human-machine interaction support the idea of a behavioral signature in children with ASD. However, several issues need to be addressed. Is this behavioral signature motoric in essence? Is it possible to ascertain that these peculiarities occur during all motor tasks (e.g. posture, voluntary movement)? Could this motor signature be considered as specific to autism, notably in comparison to DCD that also display poor motor coordination skills? We suggest that more work comparing the two conditions should be implemented, including analysis of kinematics and movement smoothness with sufficient measurement quality to allow spectral analysis.     

Developmental coordination disorder in children with attention-deficit-hyperactivity disorder and physical therapy intervention

Although physical therapy (PT) is effective in improving motor function in children with developmental coordination disorder (DCD), insufficient data are available on the impact of this intervention in children with combined attention-deficit-hyperactivity disorder (ADHD) and DCD. This prospective study aimed to establish the prevalence of DCD among a cohort of patients with ADHD, characterize the motor impairment, identify additional comorbidities, and determine the role of PT intervention on these patients. DCD was detected in 55.2% of 96 consecutive children with ADHD (81 males, 15 females), mostly among patients with the inattentive type (64.3% compared with 11% of those with the hyperactive/impulsive type, p<0.05). Mean age was 8 years 4 months (SD 2 y). Individuals with both ADHD and DCD more often had specific learning disabilities (p=0.05) and expressive language deficits (p=0.03) than children with ADHD only. Twenty-eight patients with ADHD and DCD randomly received either intensive group PT (group A, mean age 9 y 3 mo, SD 2 y 3 mo) or no intervention (group B, mean age 9 y 3 mo, SD 2 y 2 mo). PT significantly improved motor performance (assessed by the Movement Assessment Battery for Children; p=0.001). In conclusion, DCD is common in children with ADHD, particularly of the inattentive type. Patients with both ADHD and DCD are more likely to exhibit specific learning disabilities and phonological (pronunciation) deficits. Intensive PT intervention has a marked impact on the motor performance of these children.     

Age-independent and age-related deficits in visuospatial learning, sleep-wake states, thermoregulation and motor activity in PDAPP mice

Recent studies demonstrated that mice overexpressing the human mutant beta-amyloid precursor protein (hbetaAPP; PDAPP mice) show age-independent and age-related deficits in spatial learning. We used behavioral and electrophysiological techniques to determine in young and aged PDAPP mice whether deficits in spatial learning also involve alterations in sleep-wake states, thermoregulation and motor activity. Consistent with earlier studies, young PDAPP mice exhibited selective age-independent deficits using spatial, but not random and serial strategies in the circular maze. Aged PDAPP mice exhibited deficits using all search strategies. The core body temperature (Tb) in young and aged PDAPP mice was significantly lower than in age-matched non-transgenic (non-Tg) littermates. During the dark period, the motor activity (LMA) was significantly increased in young PDAPP mice, but not in aged PDAPP mice. During the light period, young PDAPP mice showed a reduction in the generation of rapid-eye-movement (REM) sleep. In contrast, aged PDAPP mice exhibited a reduction in the amount of time spent in W and an increase in SWS during the light period. Aged PDAPP mice also showed an increase in the amount of time spent in W and a reduction in REM sleep during the dark period. Our findings support previous reports indicating deficits in spatial learning in young and aged PDAPP mice. These data also suggest that PDAPP mice exhibit age-independent and age-related deficits in neural mechanisms regulating visuospatial learning, the total amount and the circadian distribution of sleep-wake states, thermoregulation and motor activity.     

Mild impairments of motor imagery skills in children with DCD

It has been hypothesized that the underlying mechanism of clumsy motor behaviour in children with Developmental Coordination Disorder (DCD) is caused by a deficit in the internal modelling for motor control. An internal modelling deficit can be shown on a behavioural level by a task that requires motor imagery. Motor imagery skills are suggested to be related to anticipatory action planning, but motor imagery and action planning have not been tested within the same child. In the present study, action planning and motor imagery skills were assessed in 82 children between 7 and 12 years of age. Twenty-one of these children met the criteria for DCD, which was assessed by the McCarron Assessment of Neuromuscular Development and 56 of these children were used in the control group. Motor imagery was tested by a mental rotation task of hands that were shown from a back and palm point of view. The results show that motor imagery is affected in children with DCD but only in conditions with complex task constraints (i.e., rotation of hand stimuli presented in palm view). These results provide partial support for the internal modelling deficit hypothesis. We were not able to elicit motor planning deficits in this group, however, and argue that more complex planning tasks may be needed to identify such deficits.     

Hemispheric specialization and functional impact of ipsilesional deficits in movement coordination and accuracy

Previous studies have demonstrated that following unilateral stroke, motor impairment occurs both contralateral, as well as ipsilateral, to the lesion. Although ipsilesional impairments can be functionally limiting, they can also provide important insight into the role of the ipsilateral hemisphere in controlling movement and the lateralization of specific motor control mechanisms, given that unilateral arm movements are thought to recruit processes in each hemisphere. The purpose of this study was to examine whether left and right hemisphere damage following stroke produces different ipsilesional deficits, and whether our dynamic dominance model of motor lateralization can predict such deficits. Specifically, the dynamic dominance model attributes control of multijoint dynamics to the left hemisphere, and control of steady-state position to the right hemisphere. Chronic stroke patients with either left or right hemisphere damage (LHD or RHD) used their ipsilesional arm, and the control subjects used either their left or right arm (LHC or RHC), to perform targeted reaching movements in different directions within the workspace ipsilateral to their reaching arm. We found that the LHD group showed deficits in controlling the arm's trajectory due to impaired multijoint coordination, but no deficits in achieving accurate final positions. In contrast, the RHD group showed deficits in final position accuracy but not in the ability to coordinate multiple joints during movement, thereby providing additional evidence for the hemisphere-specific nature of motor deficits. Furthermore, while both the LHD and RHD groups were functionally impaired to the same degree on the Jebsen Hand Function Test (JHFT), our results suggest that the underlying mechanisms for such impairment may be hemisphere-dependent.     

Differential tactile and motor recovery and cortical map alteration after C4-C5 spinal hemisection

After incomplete spinal cord injury (SCI), the adult central nervous system is spontaneously capable of substantial reorganizations that can underlie functional recovery. Most studies have focused on intraspinal reorganizations after SCI and not on the correlative cortical remodeling. Yet, differential studies of neural correlates of the recovery of sensory and motor abilities may be conducted by segregating motor and somatosensory representations in distinct and topologically organized primary cortical areas. This study was aimed at evaluating the effects of a cervical (C4-C5) spinal cord hemisection on sensorimotor performances and electrophysiological maps in primary somatosensory (S1) and motor (M1) cortices in adult rats. After SCI, an enduring loss of the affected forepaw tactile sensitivity was paralleled by the abolishment of somatosensory evoked responses in the deprived forepaw area within the S1 cortex. In contrast, severe motor deficits in unilateral forelimb were partially restored over the first postoperative month, despite remnant deficits in distal movement. The overall M1 map size was drastically reduced in SCI rats relative to intact rats. In the remaining M1 map, the shoulder and elbow movements were over-represented, consistent with the behavioral recovery of proximal joint movements in almost all rats. By contrast, residual wrist representations were observed in M1 maps of half of the rats that did not systematically correlate with a behavioral recovery of these joint movements. This study highlights the differential potential of ascending and descending pathways to reorganize after SCI.     

Prediction of recovery of motor function after stroke

BACKGROUND: Stroke is a leading cause of disability. The ability to live independently after stroke depends largely on the reduction of motor impairment and the recovery of motor function. Accurate prediction of motor recovery assists rehabilitation planning and supports realistic goal setting by clinicians and patients. Initial impairment is negatively related to degree of recovery, but inter-individual variability makes accurate prediction difficult. Neuroimaging and neurophysiological assessments can be used to measure the extent of stroke damage to the motor system and predict subsequent recovery of function, but these techniques are not yet used routinely. RECENT DEVELOPMENTS: The use of motor impairment scores and neuroimaging has been refined by two recent studies in which these investigations were used at multiple time points early after stroke. Voluntary finger extension and shoulder abduction within 5 days of stroke predicted subsequent recovery of upper-limb function. Diffusion-weighted imaging within 7 days detected the effects of stroke on caudal motor pathways and was predictive of lasting motor impairment. Thus, investigations done soon after stroke had good prognostic value. The potential prognostic value of cortical activation and neural plasticity has been explored for the first time by two recent studies. Functional MRI detected a pattern of cortical activation at the acute stage that was related to subsequent reduction in motor impairment. Transcranial magnetic stimulation enabled measurement of neural plasticity in the primary motor cortex, which was related to subsequent disability. These studies open interesting new lines of enquiry. WHERE NEXT?: The accuracy of prediction might be increased by taking into account the motor system's capacity for functional reorganisation in response to therapy, in addition to the extent of stroke-related damage. Improved prognostic accuracy could also be gained by combining simple tests of motor impairment with neuroimaging, genotyping, and neurophysiological assessment of neural plasticity. The development of algorithms to guide the sequential combinations of these assessments could also further increase accuracy, in addition to improving rehabilitation planning and outcomes.     

Learning-performance distinction and memory processes for motor skills: a focused review and perspective

Behavioral research in cognitive psychology provides evidence for an important distinction between immediate performance that accompanies practice and long-term performance that reflects the relative permanence in the capability for the practiced skill (i.e. learning). This learning-performance distinction is strikingly evident when challenging practice conditions may impair practice performance, but enhance long-term retention of motor skills. A review of motor learning studies with a specific focus on comparing differences in performance between that at the end of practice and at delayed retention suggests that the delayed retention or transfer performance is a better indicator of motor learning than the performance at (or end of) practice. This provides objective evidence for the learning-performance distinction. This behavioral evidence coupled with an understanding of the motor memory processes of encoding, consolidation and retrieval may provide insight into the putative mechanism that implements the learning-performance distinction. Here, we propose a simplistic empirically-based framework - motor behavior-memory framework - that integrates the temporal evolution of motor memory processes with the time course of practice and delayed retention frequently used in behavioral motor learning paradigms. In the context of the proposed framework, recent research has used noninvasive brain stimulation to decipher the role of each motor memory process, and specific cortical brain regions engaged in motor performance and learning. Such findings provide beginning insights into the relationship between the time course of practice-induced performance changes and motor memory processes. This in turn has promising implications for future research and practical applications.     

Review on clinical update of essential tremor

Essential tremor (ET) is considered a benign disease without any pathological changes. Nevertheless, this point of view has recently been challenged. In recent years, studies have shown that ET occurs with other non-motor symptoms, such as cognitive deficits, depression, anxiety, balance disorder, hearing impairment, olfactory dysfunction and sleep problems. Advancements in neuroimaging have revealed widespread alterations in the brain, and cerebellar involvement was the most consistent finding. In addition, studies have also shown that ET patients might experience poor quality of life, reflecting motor or non-motor symptoms. Both pharmacotherapy and non-pharmacotherapy have recently been suggested for the treatment of ET. This review briefly describes the current information on ET, including the non-movement symptoms, neuroimaging findings, the impact on daily life and ET therapy.     

A neuropsychological analysis of memory and amnesia

Drawing on neuropsychological studies of amnesic patients, cognitive studies of normal individuals, and functional neuroimaging research, this article reviews recent developments in our understanding of the cognitive and neural bases of various forms of memory. This knowledge provides a foundation for a discussion of the clinical analysis of memory disorders. Different etiologies of selective memory impairment commonly seen in neurological practice are reviewed, followed by an overview of the clinical evaluation of memory disorders. In the evaluation of memory deficits, emphasis is placed on the identification of specific processing deficits that can be linked to underlying neuropathology.