Hypothalamic Paraventricular Stimulation Inhibits Nociceptive Wide Dynamic Range Trigeminocervical Complex Cells via Oxytocinergic Transmission

Oxytocinergic transmission blocks nociception at the peripheral, spinal, and supraspinal levels through the oxytocin receptor (OTR). Indeed, a neuronal pathway from the hypothalamic paraventricular nucleus (PVN) to the spinal cord and trigeminal nucleus caudalis (Sp5c) has been described. Hence, alt...

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Published in:The Journal of neuroscience 2024-04, Vol.44 (17), p.1
Main Authors: Condés-Lara, Miguel, Martínez-Lorenzana, Guadalupe, de los Monteros-Zúñiga, Antonio Espinosa, López-Córdoba, Gustavo, Córdova-Quiroga, Aketzalli, Flores-Bojórquez, Shakty A, González-Hernández, Abimael
Format: Article
Language:English
Subjects:
Antagonists
Calcitonin
Calcitonin gene-related peptide
Cells
Chemical compounds
Dynamic range
Electrical stimuli
Electrophysiology
Fluorophores
Ganglia
Headache
Hypothalamus
Migraine
Nerves
Nucleus
Oxytocin
Pain perception
Paraventricular nucleus
Sensory neurons
Spinal cord
Stimulation
Tracers
Trigeminal ganglion
γ-Aminobutyric acid
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Summary:Oxytocinergic transmission blocks nociception at the peripheral, spinal, and supraspinal levels through the oxytocin receptor (OTR). Indeed, a neuronal pathway from the hypothalamic paraventricular nucleus (PVN) to the spinal cord and trigeminal nucleus caudalis (Sp5c) has been described. Hence, although the trigeminocervical complex (TCC), an anatomical area spanning the Sp5c, C1, and C2 regions, plays a role in some pain disorders associated with craniofacial structures (e.g., migraine), the role of oxytocinergic transmission in modulating nociception at this level has been poorly explored. Hence, in vivo electrophysiological recordings of TCC wide dynamic range (WDR) cells sensitive to stimulation of the periorbital or meningeal region were performed in male Wistar rats. PVN electrical stimulation diminished the neuronal firing evoked by periorbital or meningeal electrical stimulation; this inhibition was reversed by OTR antagonists administered locally. Accordingly, neuronal projections (using Fluoro-Ruby) from the PVN to the WDR cells filled with Neurobiotin were observed. Moreover, colocalization between OTR and calcitonin gene–related peptide (CGRP) or OTR and GABA was found near Neurobiotin-filled WDR cells. Retrograde neuronal tracers deposited at the meningeal (True-Blue, TB) and infraorbital nerves (Fluoro-Gold, FG) showed that at the trigeminal ganglion (TG), some cells were immunopositive to both fluorophores, suggesting that some TG cells send projections via the V1 and V2 trigeminal branches. Together, these data may imply that endogenous oxytocinergic transmission inhibits the nociceptive activity of second-order neurons via OTR activation in CGRPergic (primary afferent fibers) and GABAergic cells.
ISSN:0270-6474
1529-2401
1529-2401
DOI:10.1523/JNEUROSCI.1501-23.2024