Early movement restriction leads to maladaptive plasticity in the sensorimotor cortex and to movement disorders

Abstract

Motor control and body representations in the central nervous system are built, i.e., patterned, during development by sensorimotor experience and somatosensory feedback/reafference. Yet, early emergence of locomotor disorders remains a matter of debate, especially in the absence of brain damage. For instance, children with developmental coordination disorders (DCD) display deficits in planning, executing and controlling movements, concomitant with deficits in executive functions. Thus, are early sensorimotor atypicalities at the origin of long-lasting abnormal development of brain anatomy and functions? We hypothesize that degraded locomotor outcomes in adulthood originate as a consequence of early atypical sensorimotor experiences that induce developmental disorganization of sensorimotor circuitry. We showed recently that postnatal sensorimotor restriction (SMR), through hind limb immobilization from birth to one month, led to enduring digitigrade locomotion with ankle-knee overextension, degraded musculoskeletal tissues (e.g., gastrocnemius atrophy), and clear signs of spinal hyperreflexia in adult rats, suggestive of spasticity; each individual disorder likely interplaying in self-perpetuating cycles. In the present study, we investigated the impact of postnatal SMR on the anatomical and functional organization of hind limb representations in the sensorimotor cortex and processes representative of maladaptive neuroplasticity. We found that 28 days of daily SMR degraded the topographical organization of somatosensory hind limb maps, reduced both somatosensory and motor map areas devoted to the hind limb representation and altered neuronal response properties in the sensorimotor cortex several weeks after the cessation of SMR. We found no neuroanatomical histopathology in hind limb sensorimotor cortex, yet increased glutamatergic neurotransmission that matched clear signs of spasticity and hyperexcitability in the adult lumbar spinal network. Thus, even in the absence of a brain insult, movement disorders and brain dysfunction can emerge as a consequence of reduced and atypical patterns of motor outputs and somatosensory feedback that induce maladaptive neuroplasticity. Our results may contribute to understanding the inception and mechanisms underlying neurodevelopmental disorders, such as DCD.

From cerebral palsy to developmental coordination disorder: Development of preclinical rat models corresponding to recent epidemiological changes

“…It also seems to impair some executive functions in the elevated plus maze and social interactions tasks (unpublished data). Thus, in the absence of brain damage, the long-lasting locomotor disorders, hind-limb musculoskeletal histopathology, hyperreflexia and functional disorganization of the adult sensorimotor cortex, as well as signs of hyperactivity, executive dysfunctions and impairments in short-term memory, recapitulate several symptoms and neurological features observed in people with ASD and DCD in general [12,13,17,18,26,54,64].…”

“…Daily, while 335 uncasted, the hind limb joints were passively moved by the 336 investigators through their full range of motion. SMR induced a 337 growth restriction during development up to P28 but not in 338 adulthood [53,54]. 339 1.2.1.…”

“…The casts were well tolerated 332 by the pups and mothers and allowed the pups to move at the hip, 333 urinate, defecate and receive maternal care. The size of the casts 334 was adapted to the growth of the rats [51][52][53][54]. Daily, while 335 uncasted, the hind limb joints were passively moved by the 336 investigators through their full range of motion.…”

Physical therapy interventions to improve sitting ability in children with or at‐risk for cerebral palsy: a systematic review and meta‐analysis

“…2.5mo of age) advanced reaching behaviors in infants born very preterm 51 . Second, early and intensive practice provided through additional training harnesses neuroplasticity of the brain, and may also prevent the neural and functional effects of maladaptive plasticity from setting in 52 . Thus, four early intervention studies that focused on components of trunk training and postural control pertaining to sitting were included in this review.…”

Promoting sound development of preterm infants in the name of developmental neuroscience: Beyond advanced life support and neuroprotection

“…Delcour and colleagues investigated the combined effect of cerebral hypoperfusion and limb restriction, and they discovered that even in the absence of a brain insult hindlimb restriction for one month caused movement disorders and brain dysfunction. 46 The importance of motor outputs and somatosensory feedback for the sound development of infants is consistently supported by entirely different approaches. Yamada and colleagues developed an embodied brain model of a human foetus as a coupled brain-bodyenvironment system by integrating anatomical and physiological data, and they showed how intrauterine sensorimotor experiences related to bodily movements induced specific statistical regularities in somatosensory feedback that facilitated cortical learning of body representations and subsequent visual-somatosensory integration.…”