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Evidence for two subpopulations of cerebrospinal-fluid contacting neurons with opposite GABAergic signaling in adult mouse spinal cord

脑脊液 脊髓 加巴能 抑制性突触后电位 神经科学 生物 细胞生物学
作者
Priscille Riondel,Nina Jurčić,Lourdes Mounien,Stéphanie Ibrahim,Jorge Ramírez‐Franco,Sonia Stefanovic,Jérôme Trouslard,Nicolas Wanaverbecq,Riad Seddik
出处
期刊:The Journal of Neuroscience [Society for Neuroscience]
卷期号:: e2289222024-e2289222024
标识
DOI:10.1523/jneurosci.2289-22.2024
摘要

Spinal cerebrospinal fluid-contacting neurons (CSF-cNs) form an evolutionary conserved bipolar cells population localized around the central canal of all vertebrates. CSF-cNs were shown to express molecular markers of neuronal immaturity into adulthood, however the impact of their incomplete maturation on the chloride (Cl - ) homeostasis as well as GABAergic signaling remain unknown. Using adult mice from both sexes, in situ hybridization revealed that a proportion of spinal CSF-cNs (18.3%) express the Na + -K + -Cl - cotransporter 1 (NKCC1) allowing intracellular Cl - accumulation. However, we did not find expression of the K + -Cl - cotransporter 2 (KCC2) responsible for Cl - efflux in any CSF-cNs. The lack of KCC2 expression results in low Cl - extrusion capacity in CSF-cNs under high Cl - load in whole-cell patch-clamp. Using cell-attached patch-clamp allowing recordings with intact intracellular chloride concentration, we found that activation of ionotropic GABA A receptors induced both depolarizing and hyperpolarizing responses in CSF-cNs. Moreover, depolarizing GABA-responses can drive action potentials as well as intracellular calcium elevations by activating voltage-gated calcium channels. Blocking NKCC1 with bumetanide inhibited the GABA-induced calcium transients in CSF-cNs. Finally, we show that metabotropic GABA B receptors have no hyperpolarizing action on spinal CSF-cNs as their activation with baclofen did not mediate outward K + currents, presumably due to the lack of expression of G protein-coupled inwardly rectifying potassium (GIRK) channels. Together, these findings outline subpopulations of spinal CSF-cNs expressing inhibitory or excitatory GABA A receptors signaling. Excitatory GABA may promote maturation and integration of young CSF-cNs into the existing spinal circuit. Significant Statement Spinal CSF-contacting neurons (CSF-cNs) form a heterogeneous neural population with distinct maturation states in adult mice, but whether this reflects CSF-cNs with different GABAergic signaling remains unknown. Herein, we show that activation of GABA A receptors generates depolarization or hyperpolarization of CSF-cNs membrane potential in adult mouse spinal cord. Depolarizing GABA can trigger intracellular Ca 2+ elevations through the activation of voltage-gated Ca 2+ channels. Our results highlight a subpopulation of CSF-cNs in adult mice with depolarizing GABA that may promote their maturation and integration into the spinal cord.
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