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Development of kinematic and muscle patterns in preterm infants

Periodic Reporting for period 1 - INFANTPATTERNS (Development of kinematic and muscle patterns in preterm infants)

Reporting period: 2019-08-01 to 2021-07-31

INFANTPATTERNS is a cross-disciplinary project which developed and applied innovative methods at the interface of neuroscience and engineering to study the development of motor behaviour in preterm born infants.
Preterm born infants are more likely to develop long-term neurodisabilities such as cerebral palsy. Cerebral palsy often results from perinatal brain injury, is associated with a spectrum of motor impairments including poor coordination, muscle stiffness and weakness, and currently, cannot be treated. Some of this treatment failure is likely due to a fundamental lack of knowledge about early human sensorimotor development, as the evolution of motion patterns in the first months following birth has never been systematically studied. This is crucial, as motion control ultimately depends on selective muscle activation which in turn depends on control from the central nervous system.
The overall objective of INFANTPATTERNS is to create an innovative qualitative assessment and understanding of the developing motor function in preterm infants, which has high potential for significant clinical and scientific impacts. The specific aims of the project are to identify brain, kinematics, and muscle patterns during the first months following birth; and to systematically study the development of these patterns in the perinatal period.
In the newborn period, infants exhibit spontaneous but stereotyped movements of the body during which different limbs move simultaneously, known as general movements. Limb motor and sensory functions are processed in specific brain regions. The neural processing related to different body parts is reflected in patterns of functional connectivity, which in adults is strongest between brain areas corresponding to the same limb in opposite sides of the body. In INFANTPATTERNS we found that, in the brain of preterm born infants, in absence of injury, a spatial organization of functional connectivity is already present and matures across the preterm period to achieve an adult-like configuration by the normal time of birth. We also found that there is high correlation between movements of the same limb in opposite sides of the body and both limbs in the same side of the body. The patterns we identified constitute a benchmark that could be used in future to investigate if their alterations correlate with specific neurodevelopmental complications.
We also developed sensors to measure force exerted by infants and the corresponding muscle activity (known as electromyography, EMG). Mechanical flexibility and material properties make the EMG sensors suitable to comply with the delicate skin of infants. This novel technology will be used in future for the identification on muscle patterns in infants.
The human brain is organized so that specific areas of the sensorimotor cortex control or gather information from specific body parts (e.g. the limbs) (S. Dall’Orso, T. Hamstreet, S. Muceli, The “little person” in our brain who helps to direct our movements, Frontiers for Young Minds, 10:750301, 2023). In the adult brain, areas related to contralateral upper or lower limbs have a strong functional connectivity, as well as areas related to ipsilateral limbs. In INFANTPATTERNS, we analyzed functional magnetic resonance data from 400 infants born in the period corresponding to the third trimester of pregnancy. Data were collected within an ERC synergy project (319456) granted to the secondment institution (King’s College London). We found that a crude spatial organization is already present in the preterm infant somatosensory cortex and matures over the perinatal period to became similar to the organization in the adult brain (S. Dall’Orso, T. Arichi, S. P. Fitzgibbon, A. D. Edwards, E. Burdet, S. Muceli, Development of functional organization within the sensorimotor network across the perinatal period, Human Brain Mapping, 43(7): 2249-2261, 2022). Kinematic analysis of general movements of preterm infants revealed a correlation between movements from the same limb in contralateral body sides and ipsilateral upper and lower limbs.
Movement results from forces acting upon body joints. Forces are produced by muscle activation, that in turns depends on the spinal and cortical input muscles receive. Muscle activity can be recorded with high-density grids of electrodes (T. Hamstreet, S. Muceli, The pop and color of our electrified muscles, Frontiers for Young Minds, 10:742590, 2022), that allow to estimate the input muscles receive through an ad hoc signal processing method known as decomposition.
In the project, we also developed a smart biocompatible sensor for the detection of grasping force in neonates (D. Lo Presti, S. Dall’Orso, S. Muceli, T. Arichi, S. Neumane, A. Lukens, R. Sabbadini, C. Massaroni, M. A. Caponero, E. Schena, D. Formica, E. Burdet, An fMRI compatible smart device for measuring palmar grasping actions in newborns, Sensors, 20(21): 6040, 2020).
It emerged from our literature review (I. Campanini, A. Merlo, C. Disselhorst-Klug, L. Mesin, S. Muceli, R. Merletti, Fundamental concepts of bipolar and high-density surface EMG understanding and teaching for clinical, occupational and sport applications: origin, detection, and main errors, Sensors, 22(11): 4150, 2022) that when muscles have small cross-sectional areas, as in the case of children and infants, miniaturized electrodes with good electrical contact with the skin should be used. Therefore, we developed novel high-density miniaturized electrodes, that because of their mechanical flexibility and constituent material properties are highly compliant with the shape of the skin overlying small muscles. Finally, we advanced decomposition algorithms (M. Shirzadi, H. R. Marateb, K. C. McGill, S. Muceli, M. A. Mañanas, D. Farina, An accurate and real-time method for resolving superimposed action potentials in multiunit recordings, IEEE Trans Biomed Eng, 70(1): 378-389, 2023). EMG recordings will be performed in infants as possible in future.
INFANTPATTERNS provided new scientific knowledge in the field of motor development and new technology that can be used in a variety of applications. Our project described in detail the maturation of the infant sensorimotor cortex during the perinatal period, which has clear implications for both early diagnosis and management of conditions like cerebral palsy which originate in this period.
We developed novel technology for high-density surface EMG that can be used in infants and children, but also in a wide range of applications including neurophysiological research, preventive medicine, ergonomics, assessment of neurorehabilitation interventions, and human-machine interfacing.
We also produced teaching tools for training new clinical and technical operators in the field of surface EMG.