A quantitative study of neurochemically defined excitatory interneuron populations in laminae I–III of the mouse spinal cord

Gutierrez-Mecinas, Maria; Furuta, Takahiro; Watanabe, Masahiko; Todd, Andrew J

doi:10.1177/1744806916629065

Cited by 81Pain Mechanisms and TreatmentsNeuropeptides and Animal PhysiologyNeuroscience and Neuropharmacology Research

A quantitative study of neurochemically defined excitatory interneuron populations in laminae I–III of the mouse spinal cord

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Gutierrez-Mecinas, Maria, Furuta, Takahiro, Watanabe, Masahiko, Todd, Andrew J·2016·Molecular Pain

DOI 10.1177/1744806916629065PMC PMC4946630

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Abstract

Background: Excitatory interneurons account for the majority of neurons in laminae I–III, but their functions are poorly understood. Several neurochemical markers are largely restricted to excitatory interneuron populations, but we have limited knowledge about the size of these populations or their overlap. The present study was designed to investigate this issue by quantifying the neuronal populations that express somatostatin (SST), neurokinin B (NKB), neurotensin, gastrin-releasing peptide (GRP) and the γ isoform of protein kinase C (PKCγ), and assessing the extent to which they overlapped. Since it has been reported that calretinin- and SST-expressing cells have different functions, we also looked for co-localisation of calretinin and SST. Results: SST, preprotachykinin B (PPTB, the precursor of NKB), neurotensin, PKCγ or calretinin were detected with antibodies, while cells expressing GRP were identified in a mouse line (GRP-EGFP) in which enhanced green fluorescent protein (EGFP) was expressed under control of the GRP promoter. We found that SST-, neurotensin-, PPTB- and PKCγ-expressing cells accounted for 44%, 7%, 12% and 21% of the neurons in laminae I–II, and 16%, 8%, 4% and 14% of those in lamina III, respectively. GRP-EGFP cells made up 11% of the neuronal population in laminae I–II. The neurotensin, PPTB and GRP-EGFP populations showed very limited overlap, and we estimate that between them they account for ∼40% of the excitatory interneurons in laminae I–II. SST which is expressed by ∼60% of excitatory interneurons in this region, was found in each of these populations, as well as in cells that did not express any of the other peptides. Neurotensin and PPTB were often found in cells with PKCγ, and between them, constituted around 60% of the PKCγ cells. Surprisingly, we found extensive co-localisation of SST and calretinin. Conclusions: These results suggest that cells expressing neurotensin, NKB or GRP form largely non-overlapping sets that are likely to correspond to functional populations. In contrast, SST is widely expressed by excitatory interneurons that are likely to be functionally heterogeneous.

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The Prkcg dorsal excitatory family comprised Excit-3 and Excit-4 and likely corresponded to neurons involved in light static touch and allodynic pain in pathological situations.
“The Prkcg dorsal, excitatory family was comprised of Excit-3 and Excit-4 and likely corresponded to neurons involved in light static touch and allodynic pain in pathological situations46,48–56.”
From A harmonized atlas of mouse spinal cord cell types and their spatial organization (2021) · cites this paper as [53]

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Authors: Gutierrez-Mecinas, M., Furuta, T., Watanabe, M., & Todd, A. J.
Affiliations: Institute of Neuroscience and Psychology, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, UK
Kyoto University (JP)
Hokkaido University (JP)
University of Glasgow (GB)
Corresponding author: Todd, Andrew J
ORCID: Furuta, Takahiro
Watanabe, Masahiko
Todd, Andrew J
Venue: Molecular Pain
Publisher: SAGE Publications
Published: 2016-01-01
Volume: 12
Pages: 1-18
ISSN: 1744-8069 (ISSN-L)
DOI: 10.1177/1744806916629065
PMC: PMC4946630
OpenAlex: W2295921085
Cited by: 81
References: 84
Citations by year: 2026: 2 · 2025: 4 · 2024: 2 · 2023: 4 · 2022: 8 · 2021: 6 · 2020: 17 · 2019: 12 · 2018: 15 · 2017: 7 · 2016: 4
FWCI: 10.20
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by-nc
journals.sagepub.com/page/policies/text-and-data-mining-license (tdm)
Locations: Molecular Pain (publishedVersion, cc-by-nc)
PubMed Central (publishedVersion, cc-by-nc)
PubMed (publishedVersion)
ENLIGHTEN (Jurnal Bimbingan dan Konseling Islam) (acceptedVersion)
Institutional Repositories DataBase (IRDB) (submittedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Kyoto University Research Information Repository (Kyoto University) (submittedVersion, cc-by-nc)
Funders: Wellcome Trust (102645)
Japan Society for the Promotion of Science (24220007)
Topics: Health Sciences › Medicine › Physiology › Pain Mechanisms and Treatments
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords: excitatory interneurons, somatostatin, neurokinin B, neurotensin, gastrin-releasing peptide, protein kinase C gamma, calretinin, colocalization, neurochemical markers, mouse spinal cord
MeSH terms: Animals, Interneurons, Male, Mice, Inbred C57BL, Models, Biological, Neuropeptides, Neurotensin, Protein Kinase C, Protein Precursors, Somatostatin, Tachykinins, Gastrin-Releasing Peptide, Green Fluorescent Proteins, Calbindin 2, Spinal Cord Dorsal Horn

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A quantitative study of neurochemically defined excitatory interneuron populations in laminae I–III of the mouse spinal cord

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