Adult spinal motoneurons change their neurotransmitter phenotype to control locomotion

Bertuzzi, Maria; Chang, Wei‐Kuo; Ampatzis, Konstantinos

doi:10.1073/pnas.1809050115

Cited by 43 publications

(53 citation statements)

References 45 publications

(71 reference statements)

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“…In adult zebrafish and rats, there is no evidence for cholinergic descending projections from the brain to the spinal cord but only intraspinal cholinergic innervation [34][35][36] . However, to test for the possibility of transient cholinergic neurons from the brain that project to the nAChR-expressing interneurons in the spinal cord, we also examined the expression of cholinergic genes in the brain.…”

Section: Pre-and Postsynaptic Cholinergic Genes Are Expressed In the mentioning

confidence: 99%

Dynamic regulation of the cholinergic system in the spinal central nervous system

Rima

Lattouf

Younes

et al. 2020

Sci Rep

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While the role of cholinergic neurotransmission from motoneurons is well established during neuromuscular development, whether it regulates central nervous system development in the spinal cord is unclear. Zebrafish presents a powerful model to investigate how the cholinergic system is set up and evolves during neural circuit formation. In this study, we carried out a detailed spatiotemporal analysis of the cholinergic system in embryonic and larval zebrafish. In 1-day-old embryos, we show that spinal motoneurons express presynaptic cholinergic genes including choline acetyltransferase (chata), vesicular acetylcholine transporters (vachta, vachtb), high-affinity choline transporter (hacta) and acetylcholinesterase (ache), while nicotinic acetylcholine receptor (nAChR) subunits are mainly expressed in interneurons. However, in 3-day-old embryos, we found an unexpected decrease in presynaptic cholinergic transcript expression in a rostral to caudal gradient in the spinal cord, which continued during development. On the contrary, nAChR subunits remained highly expressed throughout the spinal cord. We found that protein and enzymatic activities of presynaptic cholinergic genes were also reduced in the rostral spinal cord. Our work demonstrating that cholinergic genes are initially expressed in the embryonic spinal cord, which is dynamically downregulated during development suggests that cholinergic signaling may play a pivotal role during the formation of intra-spinal locomotor circuit.

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Section: Pre-and Postsynaptic Cholinergic Genes Are Expressed In the mentioning

confidence: 99%

Dynamic regulation of the cholinergic system in the spinal central nervous system

Rima

Lattouf

Younes

et al. 2020

Sci Rep

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“…However, it must be noted that these latter studies were cross-sectional and the tested populations were elite in terms of their performance, making it difficult to separate the effect of training and heritability (Georgiades et al 2017). In conclusion, because many different plasticity mechanisms co-exist in the spinal cord (Wang & Brehm, 2017;Bertuzzi et al 2018;Chen et al 2019), short-and long-term general and task-specific adaptations most probably co-exist.…”

Section: Discussionmentioning

confidence: 99%

Motor learning induces time‐dependent plasticity that is observable at the spinal cord level

Giboin

Tokuno

Krämer

et al. 2020

The Journal of Physiology

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The spinal cord is an important contributor to motor learning r It remains unclear whether short-term spinal cord adaptations are general or task-specific r Immediately after task acquisition, neural adaptations were not specific to the trained task (i.e. were general) r Twenty-four hours after acquisition, neural adaptations appeared to be task-specific r The neural reorganization and generalization of spinal adaptations appears to be timedependent.

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“…A change in phenotype in the RVM is supported by prior literature which showed that neutral cells adopted both ON-cell and OFF-cell phenotypes after inflammation resulting in increases in both ON-cells and OFF-cells [43]. Exercise can alter neuron phenotype as evidenced by a prior study showing fast, but not slow or intermediate, motor neurons increase expression of glutamate after exercise training [2].…”

Section: Discussionmentioning

confidence: 53%

Regular physical activity reduces the percentage of spinally projecting neurons that express mu-opioid receptors from the RVM

Sluka

Kolker

Danielson

et al. 2020

Preprint

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Regular physical activity/exercise is an effective non-pharmacological treatment for individuals with chronic pain. Central inhibitory mechanisms, involving serotonin and opioids, are critical to analgesia produced by regular physical activity. The RVM sends projections to the spinal cord to inhibit or facilitate nociceptive neurons and plays a key role in exercise-induced analgesia. The goal of these studies was to examine if regular physical activity modifies RVM-spinal cord circuitry. Male and female mice received Fluoro-Gold placed on the spinal cord to identify spinally projecting neurons from the rostral ventromedial medulla (RVM) and the nucleus raphe obscuris/nucleus raphe pallidus (NRO/NRP), dermorphin-488 into caudal medulla to identify mu-opioid receptors, and were immunohistochemically stained for either phosphorylated-N-methyl-D-aspartate subunit NR1 (p-NR1) to identify excitatory neurons or tryptophan hydroxylase (TPH) to identify serotonin neurons. The percentage of dermorphin-488positive cells that stained for p-NR1 (or TPH), and the percentage of dermorphin-488positive cells that stained for p-NR1 (or TPH) and Fluoro-Gold was calculated. Physically active animals were provided running wheels in their cages for 8 weeks and compared to sedentary animals without running wheels. Animals with chronic muscle pain, induced by two intramuscular injections of pH 4.0, were compared to sham controls (pH 7.2). Physically active animals had less mu-opioid expressing neurons projecting to the spinal cord when compared to sedentary animals in the RVM, but not the NRO/NRP. No changes were observed for TPH. These data suggest that regular exercise alters central facilitation so that there is less descending facilitation to result in a net increase in inhibition. Summary Statement: Physically active animals has less mu-opioid expressing neurons projecting to the spinal cord in the RVM, but not the NRO/NRP, when compared to sedentary animals.

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Adult spinal motoneurons change their neurotransmitter phenotype to control locomotion

Cited by 43 publications

References 45 publications

Dynamic regulation of the cholinergic system in the spinal central nervous system

Dynamic regulation of the cholinergic system in the spinal central nervous system

Motor learning induces time‐dependent plasticity that is observable at the spinal cord level

Regular physical activity reduces the percentage of spinally projecting neurons that express mu-opioid receptors from the RVM

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