Abstract
Key points Many mammals are born with immature motor systems that develop through a critical period of postnatal development.In rodents, postnatal maturation of movement occurs from rostral to caudal, correlating with maturation of descending supraspinal and local spinal circuits.We asked whether development of fundamental electrophysiological properties of spinal motoneurons follows the same rostro‐caudal sequence.We show that in both regions, repetitive firing parameters increase and excitability decreases with development; however, these characteristics mature earlier in cervical motoneurons.We suggest that in addition to autonomous mechanisms, motoneuron development depends on activity resulting from their circuit milieu. Altricial mammals are born with immature nervous systems comprised of circuits that do not yet have the neuronal properties and connectivity required to produce future behaviours. During the critical period of postnatal development, neuronal properties are tuned to participate in functional circuits. In rodents, cervical motoneurons are born prior to lumbar motoneurons, and spinal cord development follows a sequential rostro‐caudal pattern. Here we asked whether birth order is reflected in the postnatal development of electrophysiological properties. We show that motoneurons of both regions have similar properties at birth and follow the same developmental profile, with maximal firing increasing and excitability decreasing into the third postnatal week. However, these maturative processes occur in cervical motoneurons prior to lumbar motoneurons, correlating with the maturation of premotor descending and local spinal systems. These results suggest that motoneuron properties do not mature by cell autonomous mechanisms alone, but also depend on developing premotor circuits.
Highlights
Altricial mammals are born with immature nervous systems comprised of circuits that have neither the neuronal properties nor connectivity required to produce future behaviours
Is this developmental trajectory maintained in the postnatal critical period such that the electrophysiological properties of cervical motoneurons are more mature at birth and fully mature before lumbar motoneurons? Or do the development and maturation of these properties rely on the development of circuits, such as descending and sensory inputs; in which case the two populations would be born with similar properties that mature as movement develops during the postnatal critical period?
We report our findings on postnatal development in each of these categories, comparing limb-innervating motoneurons within the cervical and lumbar spinal cord
Summary
Altricial mammals are born with immature nervous systems comprised of circuits that have neither the neuronal properties nor connectivity required to produce future behaviours. Cervical motoneurons are born a few days before lumbar motoneurons in mice, rats and chicks (Nornes & Das, 1974; Hollyday & Hamburger, 1977), and these regions develop sequentially from rostral to caudal (Sagner & Briscoe, 2019). Is this developmental trajectory maintained in the postnatal critical period such that the electrophysiological properties of cervical motoneurons are more mature at birth and fully mature before lumbar motoneurons? Is this developmental trajectory maintained in the postnatal critical period such that the electrophysiological properties of cervical motoneurons are more mature at birth and fully mature before lumbar motoneurons? Or do the development and maturation of these properties rely on the development of circuits, such as descending and sensory inputs; in which case the two populations would be born with similar properties that mature as movement develops during the postnatal critical period?
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