Postnatal maturation of spinal dynorphin circuits and their role in somatosensation

Brewer, Chelsie L.; Styczynski, Lauren M.; Serafin, Elizabeth K.; Baccei, Mark L.

doi:10.1097/j.pain.0000000000001884

Cited by 38Pain Mechanisms and TreatmentsNeuroscience and Neuropharmacology ResearchIon Channels and Receptors

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Postnatal maturation of spinal dynorphin circuits and their role in somatosensation

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Brewer, Chelsie L., Styczynski, Lauren M., Serafin, Elizabeth K., Baccei, Mark L.·2020·Pain

DOI 10.1097/j.pain.0000000000001884PMC PMC7509208

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Abstract

Inhibitory interneurons in the adult spinal dorsal horn (DH) can be neurochemically classified into subpopulations that regulate distinct somatosensory modalities. Although inhibitory networks in the rodent DH undergo dramatic remodeling over the first weeks of life, little is known about the maturation of identified classes of GABAergic interneurons, or whether their role in somatosensation shifts during development. We investigated age-dependent changes in the connectivity and function of prodynorphin (DYN)-lineage neurons in the mouse DH that suppress mechanosensation and itch during adulthood. In vitro patch clamp recordings revealed a developmental increase in primary afferent drive to DYN interneurons and a transition from exclusive C-fiber monosynaptic input to mixed A-fiber and C-fiber innervation. Although most adult DYN interneurons exhibited tonic firing as expected from their inhibitory phenotype, neonatal and adolescent DYN cells were predominantly classified as phasic or single-spiking. Importantly, we also found that most of the inhibitory presynaptic terminals contacting lamina I spinoparabrachial projection neurons (PNs) originate from DYN neurons. Furthermore, inhibitory synaptic input from DYN interneurons onto PNs was weaker during the neonatal period, likely reflecting a lower number of GABAergic terminals and a reduced probability of GABA release compared to adults. Finally, spinal DYN interneurons attenuated mechanical sensitivity throughout development, but this population dampened acute nonhistaminergic itch only during adulthood. Collectively, these findings suggest that the spinal “gates” controlling sensory transmission to the brain may emerge in a modality-selective manner during early life due to the postnatal tuning of inhibitory synaptic circuits within the DH.

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The Pdyn dorsal inhibitory family comprised Inhib-9, Inhib-10, and Inhib-11 and expressed markers suggestive of a role in chemical itch.
“The Pdyn dorsal, inhibitory family was comprised of Inhib-9, Inhib-10, and Inhib-11 and expressed markers suggestive of a role in chemical itch52,61,73–77.”
From A harmonized atlas of mouse spinal cord cell types and their spatial organization (2021) · cites this paper as [75]

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Authors: Brewer, C. L., Styczynski, L. M., Serafin, E. K., & Baccei, M. L.
Affiliations: University of Cincinnati (US)
University of Cincinnati Medical Center (US)
Corresponding author: Baccei, Mark L.
ORCID: Brewer, Chelsie L.
Styczynski, Lauren M.
Serafin, Elizabeth K.
Baccei, Mark L.
Venue: Pain
Publisher: Ovid Technologies (Wolters Kluwer Health)
Published: 2020-04-01
Volume: 161
Issue: 8
Pages: 1906-1924
ISSN: 0304-3959 (ISSN-L)
1872-6623
DOI: 10.1097/j.pain.0000000000001884
PMC: PMC7509208
OpenAlex: W3014548040
Cited by: 38
References: 89
Citations by year: 2026: 3 · 2025: 8 · 2024: 6 · 2023: 9 · 2022: 3 · 2021: 8 · 2020: 1
FWCI: 3.16
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Locations: Pain (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: National Institute of Neurological Disorders and Stroke (R01NS080889)
Topics: Health Sciences › Medicine › Physiology (medical) › Pain Mechanisms and Treatments
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Neuroscience › Sensory Systems › Ion Channels and Receptors
Keywords: dorsal horn, postnatal development, somatosensory perception, mechanosensing, GABAergic inhibition, presynaptic inhibition, sensory gating
MeSH terms: Animals, Dynorphins, Female, Interneurons, Male, Nerve Fibers, Myelinated, Posterior Horn Cells, Nerve Fibers, Unmyelinated, Mice, Spinal Cord Dorsal Horn

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Postnatal maturation of spinal dynorphin circuits and their role in somatosensation

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