Embryonic temporal-spatial delineation of excitatory spinal V3 interneuron diversity

• Published in: Cell reports (Cambridge) Vol. 43; no. 1; p. 113635
• Main Authors: Deska-Gauthier, Dylan, Borowska-Fielding, Joanna, Jones, Chris, Zhang, Han, MacKay, Colin S., Michail, Ramez, Bennett, Laura A., Bikoff, Jay B., Zhang, Ying
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 23.01.2024; Elsevier
• Subjects: CP: Developmental biology; CP: Neuroscience; electrophysiological profiles; Interneurons - physiology; laminar positioning; molecular diversity; morphological diversity; Movement; neurogenesis; Neurogenesis - physiology; neuronal subtypes; sensorimotor recruitment; Sim1 transcription factor; Spinal Cord; spinal locomotor circuits; spinal V3 interneurons; sensorimotor recruitment; spinal locomotor circuits; CP: Neuroscience; spinal V3 interneurons; neurogenesis; neuronal subtypes; laminar positioning; molecular diversity; CP: Developmental biology; electrophysiological profiles; Sim1 transcription factor; morphological diversity
• ISSN: 2211-1247; 2211-1247
• DOI: 10.1016/j.celrep.2023.113635

Spinal neural circuits that execute movement are composed of cardinal classes of neurons that emerged from distinct progenitor lineages. Each cardinal class contains multiple neuronal subtypes characterized by distinct molecular, anatomical, and physiological characteristics. Through a focus on the excitatory V3 interneuron class, here we demonstrate that interneuron subtype diversity is delineated through a combination of neurogenesis timing and final laminar settling position. We have revealed that early-born and late-born embryonic V3 temporal classes further diversify into subclasses with spatially and molecularly discrete identities. While neurogenesis timing accounts for V3 morphological diversification, laminar settling position accounts for electrophysiological profiles distinguishing V3 subtypes within the same temporal classes. Furthermore, V3 interneuron subtypes display independent behavioral recruitment patterns demonstrating a functional modularity underlying V3 interneuron diversity. These studies provide a framework for how early embryonic temporal and spatial mechanisms combine to delineate spinal interneuron classes into molecularly, anatomically, and functionally relevant subtypes in adults. [Display omitted] •V3 molecular subtypes are delineated through neurogenesis timing and laminar positioning•V3 axon projections emerge in temporal order following subtype-specific neurogenesis timings•V3 subtypes exhibit distinct intrinsic membrane properties by postnatal stages•V3 subtypes display overlapping, yet independent, sensorimotor recruitment patterns Deska-Gauthier et al. show that the molecular and functional diversity of V3 interneurons is delineated through a combination of embryonic neurogenesis timing and final laminar positioning. While neurogenesis timing accounted for V3 axon projection and morphological diversification, laminar position accounted for electrophysiological profiles. Furthermore, distinct V3 IN subtypes displayed independent recruitment patterns during various locomotor behaviors.