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      Long-range temporal organisation of limb movement kinematics in human neonates

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          Highlights

          • Movement occurrence is periodic in healthy newborns, with 1-hour cycle.

          • Peaks in movement occurrence associated with higher acceleration, and higher proportion of movements being bilateral.

          • Wearable sensors effectively characterise newborn movements, and have potential to be synchronised with EEG in future.

          Abstract

          Objective

          Movement provides crucial sensorimotor information to the developing brain, evoking somatotopic cortical EEG activity. Indeed, temporal-spatial organisation of these movements, including a diverse repertoire of accelerations and limb combinations (e.g. unilateral progressing to bilateral), predicts positive sensorimotor outcomes. However, in current clinical practice, movements in human neonates are qualitatively characterised only during brief periods (a few minutes) of wakefulness, meaning that the vast majority of sensorimotor experience remains unsampled. Here our objective was to quantitatively characterise the long-range temporal organisation of the full repertoire of newborn movements, over multi-hour recordings.

          Methods

          We monitored motor activity across 2–4 h in 11 healthy newborn infants (median 1 day old), who wore limb sensors containing synchronised tri-axial accelerometers and gyroscopes. Movements were identified using acceleration and angular velocity, and their organisation across the recording was characterised using cluster analysis and spectral estimation.

          Results

          Movement occurrence was periodic, with a 1-hour cycle. Peaks in movement occurrence were associated with higher acceleration, and a higher proportion of movements being bilateral.

          Conclusions

          Neonatal movement occurrence is cyclical, with periods consistent with sleep-wake behavioural architecture. Movement kinematics are organised by these fluctuations in movement occurrence. Recordings that exceed 1-hour are necessary to capture the long-range temporal organisation of the full repertoire of newborn limb movements.

          Significance

          Future work should investigate the prognostic value of combining these movement recordings with synchronised EEG, in at-risk infants.

          Related collections

          Most cited references46

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          Early motor activity drives spindle bursts in the developing somatosensory cortex.

          Sensorimotor coordination emerges early in development. The maturation period is characterized by the establishment of somatotopic cortical maps, the emergence of long-range cortical connections, heightened experience-dependent plasticity and spontaneous uncoordinated skeletal movement. How these various processes cooperate to allow the somatosensory system to form a three-dimensional representation of the body is not known. In the visual system, interactions between spontaneous network patterns and afferent activity have been suggested to be vital for normal development. Although several intrinsic cortical patterns of correlated neuronal activity have been described in developing somatosensory cortex in vitro, the in vivo patterns in the critical developmental period and the influence of physiological sensory inputs on these patterns remain unknown. We report here that in the intact somatosensory cortex of the newborn rat in vivo, spatially confined spindle bursts represent the first and only organized network pattern. The localized spindles are selectively triggered in a somatotopic manner by spontaneous muscle twitches, motor patterns analogous to human fetal movements. We suggest that the interaction between movement-triggered sensory feedback signals and self-organized spindle oscillations shapes the formation of cortical connections required for sensorimotor coordination.
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            Rapid cortical oscillations and early motor activity in premature human neonate.

            Delta-brush is the dominant pattern of rapid oscillatory activity (8-25 Hz) in the human cortex during the third trimester of gestation. Here, we studied the relationship between delta-brushes in the somatosensory cortex and spontaneous movements of premature human neonates of 29-31 weeks postconceptional age using a combination of scalp electroencephalography and monitoring of motor activity. We found that sporadic hand and foot movements heralded the appearance of delta-brushes in the corresponding areas of the cortex (lateral and medial regions of the contralateral central cortex, respectively). Direct hand and foot stimulation also reliably evoked delta-brushes in the same areas. These results suggest that sensory feedback from spontaneous fetal movements triggers delta-brush oscillations in the central cortex in a somatotopic manner. We propose that in the human fetus in utero, before the brain starts to receive elaborated sensory input from the external world, spontaneous fetal movements provide sensory stimulation and drive delta-brush oscillations in the developing somatosensory cortex contributing to the formation of cortical body maps.
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              An early marker for neurological deficits after perinatal brain lesions.

              In normal awake infants, fidgety movements are seen from the age of 6 weeks to 20 weeks. The aim of the study was to test the predictive value of absent or abnormal spontaneous movements in young infants for the later development of neurological deficits. In a collaborative study involving five hospitals we collected data on the normal and abnormal quality of fidgety movements of 130 infants and compared it with assessments of neurological development done longitudinally until the age of 2 years. On the basis of ultrasound scans infants were classified as at low-risk or at high-risk of neurological deficits. Infants were videoed for 1 h every week from birth to discharge and then for 15 min every 3 to 4 weeks; quality of general movements was assessed. Repeated neurological assessments were also done until 24 months of corrected age. 67 (96%) of 70 infants with normal fidgety movements had a normal neurological outcome. Abnormal quality or total absence of fidgety movements was followed by neurological abnormalities in 57 (95%) of the 60 infants (49 had cerebral palsy and eight had developmental retardation or minor neurological signs). Specificity and sensitivity of fidgety movement assessment were higher (96% and 95%, respectively) than of ultrasound imaging of the infants' brain (83% and 80%, respectively). Our technique of assessing spontaneous motor activity can identify and distinguish between those infants who require early intervention for neurological abnormalities and those who do not. Our technique is simple, non-intrusive, reliable, quick, and can be done on very young infants.
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                Author and article information

                Contributors
                Journal
                Clin Neurophysiol Pract
                Clin Neurophysiol Pract
                Clinical Neurophysiology Practice
                Elsevier
                2467-981X
                14 August 2020
                2020
                14 August 2020
                : 5
                : 194-198
                Affiliations
                [a ]Department of Neuroscience, Physiology and Pharmacology, University College London, London WC1E 6BT, United Kingdom
                [b ]Elizabeth Garrett Anderson Wing, University College London Hospitals, London WC1E 6DB, United Kingdom
                [c ]Division of Biokinesiology and Physical Therapy and Department of Pediatrics, University of Southern California, Los Angeles, CA 90033, United States
                Author notes
                [* ]Corresponding author at: G17 Medawar Building, University College London, Gower Street, London WC1E 6BT, United Kingdom. k.whitehead@ 123456ucl.ac.uk
                Article
                S2467-981X(20)30027-5
                10.1016/j.cnp.2020.07.007
                7493046
                b1011920-d246-43c8-9079-85c386586867
                © 2020 International Federation of Clinical Neurophysiology. Published by Elsevier B.V.

                This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).

                History
                : 2 May 2020
                : 10 July 2020
                : 26 July 2020
                Categories
                Research Paper

                motor,somatosensory,proprioception
                motor, somatosensory, proprioception

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