Intrinsic motoneuron properties in typical human development

Motoneuron properties and their firing patterns undergo significant changes throughout development and in response to neuromodulators such as serotonin. Here, we examined the age‐related development of self‐sustained firing and general excitability of tibialis anterior motoneurons in a young develop...

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Published inThe Journal of physiology Vol. 602; no. 9; pp. 2061 - 2087
Main Authors Mohammadalinejad, Ghazaleh, Afsharipour, Babak, Yacyshyn, Alex, Duchcherer, Jennifer, Bashuk, Jack, Bennett, Erin, Pearcey, Gregory E. P., Negro, Francesco, Quinlan, Katharina A., Bennett, David J., Gorassini, Monica A.
Format Journal Article
LanguageEnglish
Published England Wiley Subscription Services, Inc 01.05.2024
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Summary:Motoneuron properties and their firing patterns undergo significant changes throughout development and in response to neuromodulators such as serotonin. Here, we examined the age‐related development of self‐sustained firing and general excitability of tibialis anterior motoneurons in a young development (7–17 years), young adult (18–28 years) and adult (32–53 years) group, as well as in a separate group of participants taking selective serotonin reuptake inhibitors (SSRIs, aged 11–28 years). Self‐sustained firing, as measured by ΔF, was larger in the young development (∼5.8 Hz, n = 20) compared to the young adult (∼4.9 Hz, n = 13) and adult (∼4.8 Hz, n = 8) groups, consistent with a developmental decrease in self‐sustained firing mediated by persistent inward currents (PIC). ΔF was also larger in participants taking SSRIs (∼6.5 Hz, n = 9) compared to their age‐matched controls (∼5.3 Hz, n = 26), consistent with increased levels of spinal serotonin facilitating the motoneuron PIC. Participants in the young development and SSRI groups also had higher firing rates and a steeper acceleration in initial firing rates (secondary ranges), consistent with the PIC producing a steeper acceleration in membrane depolarization at the onset of motoneuron firing. In summary, both the young development and SSRI groups exhibited increased intrinsic motoneuron excitability compared to the adults, which, in the young development group, was also associated with a larger unsteadiness in the dorsiflexion torque profiles. We propose several intrinsic and extrinsic factors that affect both motoneuron PICs and cell discharge which vary during development, with a time course similar to the changes in motoneuron firing behaviour observed in the present study. Key points Neurons in the spinal cord that activate muscles in the limbs (motoneurons) undergo increases in excitability shortly after birth to help animals stand and walk. We examined whether the excitability of human ankle flexor motoneurons also continues to change from child to adulthood by recording the activity of the muscle fibres they innervate. Motoneurons in children and adolescents aged 7–17 years (young development group) had higher signatures of excitability that included faster firing rates and more self‐sustained activity compared to adults aged ≥18 years. Participants aged 11–28 years of age taking serotonin reuptake inhibitors had the highest measures of motoneuron excitability compared to their age‐matched controls. The young development group also had more unstable contractions, which might partly be related to the high excitability of the motoneurons. figure legend The firing behaviour of multiple, single motor units from the tibialis anterior muscle was decomposed from high‐density surface EMG to examine changes in motoneuron excitability across different phases of development from child to adulthood in 50 participants aged 7–53 years. Compared to adults (≥18 years: young adult and adult groups), motor unit discharge of children and adolescents aged 7–17 years (young development group) accelerated faster at the onset of firing, reached higher peak rates and displayed longer self‐sustained firing as represented by the amplitude of the pink boxes. Participants aged 11–28 years (red bar), taking serotonin reuptake inhibitors (SSRI) that are known to increase motoneuron excitability by facilitating persistent inward currents, had the highest measures of motoneuron excitability. High motoneuron excitability may contribute to some of the force unsteadiness during the execution of skilled ankle movements observed at the younger ages of development.
Bibliography:The peer review history is available in the Supporting Information section of this article
https://doi.org/10.1113/JP285756#support‐information‐section
Handling Editors: Richard Carson & Madeleine Lowery
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Author contributions
G.M., B.A., A.Y., F.N., K.A., DJB and MAG conceived and designed research. G.M., B.A., A.Y., J.D. and MAG performed experiments. G.M., B.A., A.Y., J.D., J.B., E.B., GEP and MAG analysed the data. G.M., B.A., Y.A., GEP, K.A., DJB and MAG interpreted the results of experiments. G.M., J.N., A.Y., GEP and MAG prepared figures. G.M., GEP and MAG drafted and revised the manuscript and all authors edited the manuscript. All authors approved the final version of the manuscriupt submitted for pub;ication. All authors agree to be accountable for all aspects of the work. The authors confirm that all persons designated as authors are qualified.
ISSN:0022-3751
1469-7793
1469-7793
DOI:10.1113/JP285756