Motor deficits in autism differ from that of developmental coordination disorder.

LAY ABSTRACT: A vast majority of individuals with autism spectrum disorder experience impairments in motor skills. Those are often labelled as additional developmental coordination disorder despite the lack of studies comparing both disorders. Consequently, motor skills rehabilitation programmes in autism are often not specific but rather consist in standard programmes for developmental coordination disorder. Here, we compared motor performance in three groups of children: a control group, an autism spectrum disorder group and a developmental coordination disorder group. Despite similar level of motor skills evaluated by the standard movement assessment battery for children, in a Reach-to-Displace Task, children with autism spectrum disorder and developmental coordination disorder showed specific motor control deficits. Children with autism spectrum disorder failed to anticipate the object properties, but could correct their movement as well as typically developing children. In contrast, children with developmental coordination disorder were atypically slow, but showed a spared anticipation. Our study has important clinical implications as motor skills rehabilitations are crucial to both populations. Specifically, our findings suggest that individuals with autism spectrum disorder would benefit from therapies aiming at improving their anticipation, maybe through the support of their preserved representations and use of sensory information. Conversely, individuals with developmental coordination disorder would benefit from a focus on the use of sensory information in a timely fashion.

A Somatosensory Computation That Unifies Limbs and Tools.

It is often claimed that tools are embodied by their user, but whether the brain actually repurposes its body-based computations to perform similar tasks with tools is not known. A fundamental computation for localizing touch on the body is trilateration. Here, the location of touch on a limb is computed by integrating estimates of the distance between sensory input and its boundaries (e.g., elbow and wrist of the forearm). As evidence of this computational mechanism, tactile localization on a limb is most precise near its boundaries and lowest in the middle. Here, we show that the brain repurposes trilateration to localize touch on a tool, despite large differences in initial sensory input compared with touch on the body. In a large sample of participants, we found that localizing touch on a tool produced the signature of trilateration, with highest precision close to the base and tip of the tool. A computational model of trilateration provided a good fit to the observed localization behavior. To further demonstrate the computational plausibility of repurposing trilateration, we implemented it in a three-layer neural network that was based on principles of probabilistic population coding. This network determined hit location in tool-centered coordinates by using a tool's unique pattern of vibrations when contacting an object. Simulations demonstrated the expected signature of trilateration, in line with the behavioral patterns. Our results have important implications for how trilateration may be implemented by somatosensory neural populations. We conclude that trilateration is likely a fundamental spatial computation that unifies limbs and tools.

Up right, not right up: Primacy of verticality in both language and movement.

When describing motion along both the horizontal and vertical axes, languages from different families express the elements encoding verticality before those coding for horizontality (e.g., going up right instead of right up). In light of the motor grounding of language, the present study investigated whether the prevalence of verticality in Path expression also governs the trajectory of arm biological movements. Using a 3D virtual-reality setting, we tracked the kinematics of hand pointing movements in five spatial directions, two of which implied the vertical and horizontal vectors equally (i.e., up right +45° and bottom right -45°). Movement onset could be prompted by visual or auditory verbal cues, the latter being canonical in French ("en haut à droite"/up right) or not ("à droite en haut"/right up). In two experiments, analyses of the index finger kinematics revealed a significant effect of gravity, with earlier acceleration, velocity, and deceleration peaks for upward (+45°) than downward (-45°) movements, irrespective of the instructions. Remarkably, confirming the linguistic observations, we found that vertical kinematic parameters occurred earlier than horizontal ones for upward movements, both for visual and congruent verbal cues. Non-canonical verbal instructions significantly affected this temporal dynamic: for upward movements, the horizontal and vertical components temporally aligned, while they reversed for downward movements where the kinematics of the vertical axis was delayed with respect to that of the horizontal one. This temporal dynamic is so deeply anchored that non-canonical verbal instructions allowed for horizontality to precede verticality only for movements that do not fight against gravity. Altogether, our findings provide new insights into the embodiment of language by revealing that linguistic path may reflect the organization of biological movements, giving priority to the vertical axis.

Body schema plasticity is altered in Developmental Coordination Disorder.

Developmental Coordination Disorder (DCD) is a pathological condition characterized by impaired motor skills. Current theories advance that a deficit of the internal models is mainly responsible for DCD children's altered behavior. Yet, accurate movement execution requires not only correct movement planning, but also integration of sensory feedback into body representation for action (Body Schema) to update the state of the body. Here we advance and test the hypothesis that the plasticity of this body representation is altered in DCD. To probe Body Schema (BS) plasticity, we submitted a well-established tool-use paradigm to seventeen DCD children, required to reach for an object with their hand before and after tool use, and compared their movement kinematics to that of a control group of Typically Developing (TD) peers. We also asked both groups to provide explicit estimates of their arm length to probe plasticity of their Body Image (BI). Results revealed that DCD children explicitly judged their arm shorter after tool use, showing changes in their BI comparable to their TD peers. Unlike them, though, DCD did not update their implicit BS estimate: kinematics showed that tool use affected their peak amplitudes, but not their latencies. Remarkably, the kinematics of tool use showed that the motor control of the tool was comparable between groups, both improving with practice, confirming that motor learning abilities are preserved in DCD. This study thus brings evidence in favor of an alternative theoretical account of the DCD etiology. Our findings point to a deficit in the plasticity of the body representation used to plan and execute movements. Though not mutually exclusive, this widens the theoretical perspective under which DCD should be considered: DCD may not be limited to a problem affecting the internal models and their motor functions, but may concern the state of the effector they have to use.

Tool use and language share syntactic processes and neural patterns in the basal ganglia.

Does tool use share syntactic processes with language? Acting with a tool is thought to add a hierarchical level into the motor plan. In the linguistic domain, syntax is the cognitive function handling interdependent elements. Using functional magnetic resonance imaging, we detected common neurofunctional substrates in the basal ganglia subserving both tool use and syntax in language. The two abilities elicited similar patterns of neural activity, indicating the existence of shared functional resources. Manual actions and verbal working memory did not contribute to this common network. Consistent with the existence of shared neural resources, we observed bidirectional behavioral enhancement of tool use and syntactic skills in language so that training one function improves performance in the other. This reveals supramodal syntactic processes for tool use and language.

The toolish hand illusion: embodiment of a tool based on similarity with the hand.

A tool can function as a body part yet not feel like one: Putting down a fork after dinner does not feel like losing a hand. However, studies show fake body-parts are embodied and experienced as parts of oneself. Typically, embodiment illusions have only been reported when the fake body-part visually resembles the real one. Here we reveal that participants can experience an illusion that a mechanical grabber, which looks scarcely like a hand, is part of their body. We found changes in three signatures of embodiment: the real hand's perceived location, the feeling that the grabber belonged to the body, and autonomic responses to visible threats to the grabber. These findings show that artificial objects can become embodied even though they bear little visual resemblance to the hand.

The long developmental trajectory of body representation plasticity following tool use.

Humans evolution is distinctly characterized by their exquisite mastery of tools, allowing them to shape their environment in more elaborate ways compared to other species. This ability is present ever since infancy and most theories indicate that children become proficient with tool use very early. In adults, tool use has been shown to plastically modify metric aspects of the arm representation, as indexed by changes in movement kinematics. To date, whether and when the plastic capability of updating the body representation develops during childhood remains unknown. This question is particularly important since body representation plasticity could be impacted by the fact that the human body takes years to achieve a stable metric configuration. Here we assessed the kinematics of 90 young participants (8-21 years old) required to reach for an object before and after tool use, as a function of their pubertal development. Results revealed that tool incorporation, as indexed by the adult typical kinematic pattern, develops very slowly and displays a u-shaped developmental trajectory. From early to mid puberty, the changes in kinematics following tool use seem to reflect a shortened arm representation, opposite to what was previously reported in adults. This pattern starts reversing after mid puberty, which is characterized by the lack of any kinematics change following tool use. The typical adult-like pattern emerges only at late puberty, when body size is stable. These findings reveal the complex dynamics of tool incorporation across development, possibly indexing the transition from a vision-based to a proprioception-based body representation plasticity.

Elementary visuospatial perception deficit in children with neurodevelopmental disorders.

AIM: To assess the prevalence of elementary visuospatial perception (EVSP) deficit in children with neurodevelopmental disorders. METHOD: Using a screening test designed and validated to measure dorsal EVSP ability, 168 children (122 males, 46 females; mean age 10y [SD 1y 10mo], range 4y 8mo-16y 4mo) diagnosed with developmental coordination disorder (DCD), specific learning disorder (SLD), attention-deficit/hyperactivity disorder (ADHD), and/or oral language disorder were compared with a group of 184 typically developing children. We also tested 14 children with binocular vision dysfunction and no neurodevelopmental disorder. RESULTS: Children with SLD scored below the interquartile range of typically developing children as frequently (59%) as children with DCD, but only 5% were severely impaired (i.e. scored as outliers). Children with DCD were the most severely impaired (22% of outliers), even more so when they exhibited a co-occuring disorder. Children with language disorder and those with binocular vision dysfunction scored similarly to the group of typically developing children. INTERPRETATION: These results confirm the importance of assessing EVSP in the clinical evaluation of children with neurodevelopmental disorders, in particular those presenting with DCD or SLD. What this paper adds More than half of children with developmental coordination disorder (DCD) scored below the normal interquartile range on the elementary visuospatial perception (EVSP) test. More than half of children with specific learning disorder (SLD) scored below the normal interquartile range on the EVSP test. Twenty-two percent of children with DCD performed as outliers on the EVSP test. Children with language disorder and those with binocular vision dysfunction scored similarly to typically developing children.

Online proprioception feeds plasticity of arm representation following tool-use in healthy aging.

Following tool-use, the kinematics of free-hand movements are altered. This modified kinematic pattern has been taken as a behavioral hallmark of the modification induced by tool-use on the effector representation. Proprioceptive inputs appear central in updating the estimated effector state. Here we questioned whether online proprioceptive modality that is accessed in real time, or offline, memory-based, proprioception is responsible for this update. Since normal aging affects offline proprioception only, we examined a group of 60 year-old adults for proprioceptive acuity and movement's kinematics when grasping an object before and after tool-use. As a control, participants performed the same movements with a weight-equivalent to the tool-weight-attached to their wrist. Despite hampered offline proprioceptive acuity, 60 year-old participants exhibited the typical kinematic signature of tool incorporation: Namely, the latency of transport components peaks was longer and their amplitude reduced after tool-use. Instead, we observed no kinematic modifications in the control condition. In addition, online proprioception acuity correlated with tool incorporation, as indexed by the amount of kinematics changes observed after tool-use. Altogether, these findings point to the prominent role played by online proprioception in updating the body estimate for the motor control of tools.

Feeling better: Tactile verbs speed up tactile detection.

Embodiment of action-related language into the motor system has been extensively documented. Yet the case of sensory words, especially referring to touch, remains overlooked. We investigated the influence of verbs denoting tactile sensations on tactile perception. In Experiment 1, participants detected tactile stimulations on their forearm, preceded by tactile or non-tactile verbs by one of three delays (170, 350, 500 ms) reflecting different word processing stages. Results revealed shorter reaction times to tactile stimulations following tactile than non-tactile verbs, irrespective of delay. To ensure that priming pertained to tactile, and not motor, verb properties, Experiment 2 compared the impact of tactile verbs to both action and non-tactile verbs, while stimulations were delivered on the index finger. No priming emerged following action verbs, therefore not supporting the motor-grounded interpretation. Facilitation by tactile verbs was however not observed, possibly owing to methodological changes. Experiment 3, identical to Experiment 2 except that stimulation was delivered to participants' forearm, replicated the priming effect. Importantly, tactile stimulations were detected faster after tactile than after both non-tactile and action verbs, indicating that verbs' tactile properties engaged resources shared with sensory perception. Our findings suggest that language conveying tactile information can activate somatosensory representations and subsequently promote tactile detection.

Highs and Lows in Motor Control Development.

Motor control is classically described as relying on two components: anticipatory control (feedforward processing) and online control (feedback processing). Here we aimed to unveil the developmental steps of both feedback and feedforward control in 5-10 years old children, using a simple and ecological task. We manipulated object's weight in a reach-to-displace paradigm. When the weight was known before lifting it, anticipatory processes were quantifiable during the reaching phase. Conversely, an unknown weight triggered online corrections during the displacing phase. Movement kinematics revealed that children anticipate this objet property as young as 5 y-o. This anticipation becomes adequate around 7 y-o and is paralleled by poor online corrections. This simple yet relevant paradigm should allow quantifying deviations from neurotypical patterns in disorders of motor control.

Validation of a simple screening test for elementary visuo-spatial perception deficit.

OBJECTIVE: The reliability and validity of a screening test for a deficit in elementary visuo-spatial perception (EVSP) were evaluated. METHOD: This prospective study collected performance from 210 typically developing individuals and evaluated the internal consistency of the EVSP screening test. Test-retest reliability was examined with 25 individuals. Validity also involved retrospective clinical data collected from 223 non-typically developing children coming to the hospital for outpatient consultation. Since EVSP matures through childhood, we standardized the EVSP screening test scores by age category and performed Pearson correlations with standardized clinical tests scores. RESULTS: Test-retest reliability (intraclass correlation coefficient=0.76) and internal consistency (Cronbach's alpha=0.76) were satisfactory. Construct validity included correlation with the subtests of the Wechsler Intelligence Scale IV (WISC-IV) involving visuo-spatial analysis (Matrix Reasoning and Block Design, P<0.01; Symbol Search and Coding, P<0.05) and was reinforced by the expected non-correlation between the Verbal Comprehension Index and EVSP scoring class. The EVSP scoring class was correlated with Manual dexterity of the M-ABC (P<0.05) and the Working Memory Index (P<0.05) of the WISC-IV including the subtest Arithmetic (P<0.01). CONCLUSION: This screening test is reliable and valid to evaluate EVSP before more complex cognitive or motor assessment.

Language as a Tool: Motor Proficiency Using a Tool Predicts Individual Linguistic Abilities.

Different disciplines converge to trace language evolution from motor skills. The human ability to use tools has been advocated as a fundamental step toward the emergence of linguistic processes in the brain. Neuropsychological and neuroimaging research has established that linguistic functions and tool-use are mediated by partially overlapping brain networks. Yet, scholars still theoretically debate whether the relationship between tool-use and language is contingent or functionally relevant, since empirical evidence is critically missing. Here, we measured both linguistic production and tool-use abilities in the same participants, as well as manual and linguistic motor skills. A path analysis ruling out unspecific contributions from manual or linguistic motor skills, showed that motor proficiency using a tool lawfully predicts differences in individual linguistic production. In addition, more complex tool-use reveals stronger association between linguistic production and tool mastery. These findings establish the existence of shared cognitive processes between tool-use and language.

Tracking the acquisition of anticipatory postural adjustments during a bimanual load-lifting task: A MEG study.

During bimanual coordination, that is, manipulating with the dominant hand an object held by the postural hand, anticipatory postural adjustments are required to cancel the perturbations and ensure postural stabilization. Using magnetoencephalography (MEG), we investigated changes mediating the acquisition of anticipatory postural adjustments during a bimanual load-lifting task. Participants lifted a load with their right hand, hence triggering the fall of a second load fixed to their left (postural) forearm. During Acquisition, the onset of load-lifting and the fall of the second load were experimentally delayed after few trials. During Control, load-lifting triggered the fall of the second load without delay. Upward elbow rotation decreased with trial repetition during Acquisition, hence attesting the ongoing acquisition of anticipatory postural adjustments. Bilateral event-related desynchronisation (ERD) of the alpha rhythm (8-12 Hz) was recorded. Generators of the mu rhythm were found within central and associative motor regions. Their spatial distribution within the hemisphere contralateral to the load-lifting arm was less refined and circumscribed during Acquisition compared to Control. Regression analyses emphasized the specific involvement of the precuneus in the right hemisphere contralateral to the postural forearm, and a medial prefrontal region in the left hemisphere. Analyses of the time course power showed that an increase in preunloading activation within the precuneus and a decrease in postunloading inhibition within the medial prefrontal region were associated with the acquisition of anticipatory postural adjustments. The study provides original insights into cortical activations mediating the progressive tuning of anticipatory postural adjustments during the acquisition stage of motor learning.

Basal ganglia involvement in ARX patients: The reason for ARX patients very specific grasping?

The ARX (Aristaless Related homeoboX) gene was identified in 2002 as responsible for XLAG syndrome, a lissencephaly characterized by an almost complete absence of cortical GABAergic interneurons, and for milder forms of X-linked Intellectual Disability (ID) without apparent brain abnormalities. The most frequent mutation found in the ARX gene, a duplication of 24 base pairs (c.429_452dup24) in exon 2, results in a recognizable syndrome in which patients present ID without primary motor impairment, but with a very specific upper limb distal motor apraxia associated with a pathognomonic hand-grip, described as developmental Limb Kinetic Apraxia (LKA). In this study, we first present ARX expression during human fetal brain development showing that it is strongly expressed in GABAergic neuronal progenitors during the second and third trimester of pregnancy. We show that although ARX expression strongly decreases towards the end of gestation, it is still present after birth in some neurons of the basal ganglia, thalamus and cerebral cortex, suggesting that ARX also plays a role in more mature neuron functioning. Then, using morphometric brain MRI in 13 ARX patients carrying c.429_452dup24 mutation and in 13 sex- and age-matched healthy controls, we show that ARX patients have a significantly decreased volume of several brain structures including the striatum (and more specifically the caudate nucleus), hippocampus and thalamus as well as decreased precentral gyrus cortical thickness. We observe a significant correlation between caudate nucleus volume reduction and motor impairment severity quantified by kinematic parameter of precision grip. As basal ganglia are known to regulate sensorimotor processing and are involved in the control of precision gripping, the combined decrease in cortical thickness of primary motor cortex and basal ganglia volume in ARX dup24 patients is very likely the anatomical substrate of this developmental form of LKA.

Proprioception Is Necessary for Body Schema Plasticity: Evidence from a Deafferented Patient.

The ability of using a large variety of tools is important in our daily life. Behind human tool-use abilities lays the brain capacity to incorporate tools into the body representation for action (Body Schema, BS), thought to rely mainly on proprioceptive information. Here, we tested whether tool incorporation is possible in absence of proprioception by studying a patient with right upper-limb deafferentation. We adopted a paradigm sensitive to changes of the BS and analyzed the kinematics of free-hand movements before and after tool-use, in three sessions over a period of 2 years. In the first session, before tool-use, the kinematics of the deafferented hand was disrupted. Similarly, the first movements with the tool (a mechanical grabber elongating the arm by ~40 cm) showed an abnormal profile that tended to normalize at the end of the session. Subsequent free-hand movements were also normalized. At session 2, 6 months later, the patient exhibited normal free-hand kinematic profiles, additionally showing changes in grasping kinematics after tool-use, but no sign of tool incorporation. A follow-up 2 years later, further confirmed the normalized kinematic profile but the absence of tool incorporation. This first description of tool-use in absence of proprioception shows the fundamental role of proprioception in the update of the BS. These results provide an important further step in understanding human motor control and have implications for future development of rehabilitation programs for patients with sensory deficits.

Tool-use: An open window into body representation and its plasticity.

Over the last decades, scientists have questioned the origin of the exquisite human mastery of tools. Seminal studies in monkeys, healthy participants and brain-damaged patients have primarily focused on the plastic changes that tool-use induces on spatial representations. More recently, we focused on the modifications tool-use must exert on the sensorimotor system and highlighted plastic changes at the level of the body representation used by the brain to control our movements, i.e., the Body Schema. Evidence is emerging for tool-use to affect also more visually and conceptually based representations of the body, such as the Body Image. Here we offer a critical review of the way different tool-use paradigms have been, and should be, used to try disentangling the critical features that are responsible for tool incorporation into different body representations. We will conclude that tool-use may offer a very valuable means to investigate high-order body representations and their plasticity.

Changing ideas about others' intentions: updating prior expectations tunes activity in the human motor system.

Predicting intentions from observing another agent's behaviours is often thought to depend on motor resonance - i.e., the motor system's response to a perceived movement by the activation of its stored motor counterpart, but observers might also rely on prior expectations, especially when actions take place in perceptually uncertain situations. Here we assessed motor resonance during an action prediction task using transcranial magnetic stimulation to probe corticospinal excitability (CSE) and report that experimentally-induced updates in observers' prior expectations modulate CSE when predictions are made under situations of perceptual uncertainty. We show that prior expectations are updated on the basis of both biomechanical and probabilistic prior information and that the magnitude of the CSE modulation observed across participants is explained by the magnitude of change in their prior expectations. These findings provide the first evidence that when observers predict others' intentions, motor resonance mechanisms adapt to changes in their prior expectations. We propose that this adaptive adjustment might reflect a regulatory control mechanism that shares some similarities with that observed during action selection. Such a mechanism could help arbitrate the competition between biomechanical and probabilistic prior information when appropriate for prediction.

Grasping objects by former amputees: The visuo-motor control of allografted hands.

PURPOSE: Hand allograft has recently emerged as a therapeutic option for upper limb amputees. Functional neuroimaging studies have progressively revealed sensorimotor cortices plasticity following both amputation and transplantation. The purpose of our study was to assess and characterize the functional recovery of the visuo-motor control of prehension in bilateral hand transplanted patients. METHODS: Using kinematics recordings, we characterized the performance of prehension with or without visual feed-back for object of different position and size, in five bilateral hand allograft recipients and age-matched control subjects. Both hands were assessed, separately. RESULTS: Despite an overall slower execution, allografted patients succeeded in grasping for more than 90% of the trials. They exhibited a preserved hand grip scaling according to object size, and preserved prehension performances when tested without visual feedback. These findings highlight the allograft recipients' abilities to produce an effective motor program, and a good proprioceptive-dependent online control. Nevertheless, the maximum grip aperture was reduced and delayed, the coupling between Transport and Grasp components was altered, and the final phase of the movement was lengthened. CONCLUSION: Hand allotransplantation can offer recipients a good recovery of the visuo-motor control of prehension, with slight impairments likely attributable to peripheral neuro-orthopedic limitations.

Tool use imagery triggers tool incorporation in the body schema.

Tool-use has been shown to modify the way the brain represents the metrical characteristics of the effector controlling the tool. For example, the use of tools that elongate the physical length of the arm induces kinematic changes affecting selectively the transport component of subsequent free-hand movements. Although mental simulation of an action is known to involve -to a large extent- the same processes as those at play in overt motor execution, whether tool-use imagery can yield similar effects on the body representation remains unknown. Mentally simulated actions indeed elicit autonomic physiological responses and follow motor execution rules that are comparable to those associated with the correspondent overt performance. Therefore, here we investigated the effects of the mental simulation of actions performed with a tool on the body representation by studying subsequent free-hand movements. Subjects executed reach to grasp movements with their hand before and after an imagery task performed with either a tool elongating their arm length or, as a control, with their hand alone. Two main results were found: First, in agreement with previous studies, durations of imagined movements performed with the tool and the hand were similarly affected by task difficulty. Second, kinematics of free-hand movements was affected after tool-use imagery, but not hand-use imagery, in a way similar to that previously documented after actual tool-use. These findings constitute the first evidence that tool-use imagery is sufficient to affect the representation of the user's arm.