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.
Highlights
It is understood that development of movement repertoires, motor control and body representations in sensorimotor circuitry are achieved through early spontaneous movements, sensorimotor experiences and reafference in children[1,2,3] and rodents[4,5]
We used 17 rats that were exposed to sensorimotor restriction (SMR; Fig. 1) and 20 control rats of either sex
To investigate a hypothesis of a developmental origin of adult disorders, we showed in the present study that reduced and abnormal patterns of somatosensory inputs after hind limb movement restriction during postnatal development had no significant impact on adult brain neuroanatomy yet did effect the functional organization of the sensorimotor cortex
Summary
It is understood that development of movement repertoires, motor control and body representations in sensorimotor circuitry are achieved through early spontaneous movements, sensorimotor experiences and reafference in children[1,2,3] and rodents[4,5]. We hypothesized that limited and abnormal patterns of somatosensory inputs during development may lead to abnormal anatomical and functional organization of the sensorimotor circuitry in adulthood as a result of maladaptive cortical plasticity Such sensorimotor disorganization may in turn alter somatosensory and bodily perceptions, motor outputs, and musculoskeletal structure and physiology. We postulated that reduced and atypical patterns of both motor outputs and somatosensory reafference during development likely contributed to the emergence of movement disorders and musculoskeletal pathologies that persisted into adulthood[23] To further explore this concept that adult movement disorders may have developmental origins even in the absence of brain damage, we investigated here the impact of postnatal SMR on the neuroanatomical and functional organization of hind limb somatosensory and motor representations in adult rats using microelectrode cortical mapping techniques, and brain histology and immunochemistry. To further understand the processes and interactions underlying any maladaptive neural plasticity, we performed principal components analyses (PCA) to summarize the many variables recorded within the same animals and linear correlations between these variables
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