Calcitonin gene-related peptide containing sympathetic preganglionic and sensory neurons projecting to the superior cervical ganglion of the rat

doi:10.1016/0006-8993(89)90952-9

Brain Research

Volume 487, Issue 1, 15 May 1989, Pages 158-164

https://doi.org/10.1016/0006-8993(89)90952-9 Get rights and content

Abstract

The origin of calcitonin gene-related peptide (CGRP)-containing fibers observed in the superior cervical ganglia (SCG) of the rat was investigated by a combined technique of retrograde axonal tracing and indirect immunofluorescence. Following the injection of Fast blue (FB) into the SCG, labeled neurons were observed in the C₈-T₅ spinal cord segments, with the highest density in T₁-T₃ (5–8 neurons per section). More than 90% of them were located in the ipsilateral intermediolateral cell column (IML) and the rest were found in the central autonomic area (CA) and intercalated region (IC) between the IML and CA. CGRP-like immunoreactive (IR) neurons were detected in these areas in animals pretreated with colchicine. About one-fourth of FB-labeled cells were CGRP-IR, which corresponded to three-fourths of the CGRP-IR neurons in the above-mentioned autonomic areas of these spinal cord segments. Most of these double-labeled cells were found in the IML (95%). A few FB-labeled cells were also observed in dorsal root ganglia (C₈-T₅) and 30% of them were CGRP-IR. These findings suggested that the CGRP-IR fibers in the rats SCG are supplied from both sympathetic preganglionic neurons in the spinal cord and sensory ganglion cells, although the latter projection is quite rare.

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Source and origin of nerve fibres immunoreactive for substance P and calcitonin gene-related peptide in the normal and chronically denervated superior cervical sympathetic ganglion of the rat
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Citation Excerpt :
These newly formed nerve fibres form synapses, which are capable of stimulant triggered exocytosis, upon the ganglionic neurones (Zaidi and Matthews, 1999). Foregoing immunohistochemical studies of sympathetic ganglia have indicated that the normal rat SCG contains both SP-IR and CGRP-IR fibres (SP: Hökfelt et al., 1977; Heym et al., 1993a,b; CGRP: Yamamoto et al., 1989; Heym et al., 1993a). There are more CGRP-IR fibres than SP-IR fibres; and CGRP- and SP-immunoreactivity coexist in some fibres.
Immunohistochemical studies of sympathetic ganglia have indicated that the normal rat superior cervical ganglion contains both SP-IR and CGRP-IR fibres, and CGRP- and SP-immunoreactivity coexist in some fibres. In rat sympathetic ganglia decentralization by preganglionic denervation leads to intraganglionic increase of peptidergic fibres immunoreactive (IR) for substance P (SP) and calcitonin gene-related peptide. We explored the sources of SP- and CGRP-IR fibres in normal and in chronically decentralized rat SCGs.
The distribution of immunoreactivities for CGRP and SP was determined in SCGs of normal rats and of rats following preganglionic denervation followed by sensory denervation. Ganglia were studied after short-term (2–5 days) sensory denervation, and long-term (7–16 months) sympathetic denervation followed by short-term (2 days) sensory denervation. To explore for the production of SP and CGRP by intrinsic neurones within the ganglion, normal and chronically decentralized SCGs were examined following pretreatment by local in vivo application of colchicine. Normal and chronically decentralized ganglia were also injected with fluorescent tracer Fluorogold for retrograde tracing of extrinsic fibres back to their neurones of origin.
The observations suggest that in normal SCG in the rat the SP-IR and CGRP-IR nerve fibres are derived via direct links from vagus and glossopharyngeal nerves and the cervical plexus, or from nerve fibres running along the cervical sympathetic trunk, and the external carotid and the internal carotid nerves.
Sensory nerve inputs to the rat SCG following decentralization may contribute to the low levels of ganglionic activation observable in the autonomic failure of multiple system atrophy in man.
Cervical sympathectomy reduces neurogenic vasodilation in dura mater of rats
2011, Autonomic Neuroscience: Basic and Clinical
Citation Excerpt :
Blockade of CGRP receptors leads to the inhibition of stimulus-induced vasodilation in dura mater (Dux et al., 2003). CGRP-immunoreactive preganglionic neurons have been found in the intermediolateral nucleus of the rat, and CGRP-positive nerve fibers were absent from the rat sympathetic nerve after preganglionic transection of the sympathetic trunk (Yamamoto et al., 1989). Therefore, is meningeal blood flow reduction caused by sympathetic blockade due to the reduced release of CGRP?
Migraine may affect the autonomic nervous system, but the mechanisms remain unclear. The sympathetic and parasympathetic nervous systems may play different roles in the attack. To explore the effect of blocking the cervical sympathetic nerve on vasodilation of the meningeal vessels, jugular vein calcitonin gene-related peptide (CGRP) and meningeal blood flow changes were measured before and after transection of the cervical sympathetic nerve by electrically stimulating the trigeminal ganglion in Sprague–Dawley (SD) rats. We found that CGRP level and meningeal blood flow increased in both the sham-operated and sympathectomized groups (p < 0.05). Compared with the sham-operated group, dural blood flow decreased significantly in the cervical sympathectomy group, but CGRP level was not significantly different between these two groups. The cervical sympathetic nerve may play an important role in the process of neurogenic dural vasodilation in rats; this effect is not entirely dependent on CGRP level.
Morphological and immunohistochemical characterization of the trigeminal ganglion neurons innervating the cornea and upper eyelid of the rat
2007, Journal of Chemical Neuroanatomy
The cornea is sensitive to nociceptive stimuli and receives dense sensory innervations from the trigeminal ganglion, which also innervates the upper eyelid. We investigated the morphological and immunohistochemical characterization of the trigeminal ganglion neurons innervating the cornea and upper eyelid. We injected the retrograde tracer Fluoro-Gold (FG) into the cornea and the retrograde tracer cholera toxin subunit b (CTb) into the upper eyelid of the same animal. Less than 10% of the FG-labeled neurons were also labeled with CTb. The FG-labeled neurons were small (29.6 ± 0.6 μm), while the CTb-labeled neurons were large (36.1 ± 0.5 μm). We also characterized the neurons in the trigeminal ganglion with the retrograde tracer FG following its injection into the cornea or the upper eyelid, and immunohistochemical double-labeling with nociception-related neuronal markers, such as calcitonin gene-related peptides (CGRP), transient receptor potentiated vanilloid 1 (TRPV1), and substance P (SP). About 27% of the neurons innervating the cornea were double-labeled with CGRP, about 23% with TRPV1, and about 8% with SP. About 4% of the neurons innervating the upper eyelid were double-labeled for CGRP, about 11% for TRPV1, and 3% for SP. Thus, the percentages of double-labeled neurons for the neurons innervating the cornea were higher than those for the neurons innervating the upper eyelid. These results indicate that the cornea and the upper eyelid receive innervations mainly from different neurons of the trigeminal ganglia. The cornea is innervated by many characteristic sensory neurons containing nociception-related neuronal markers.
Role of CGRP and GABA in the hypotensive effect of intrathecally administered anandamide to anesthetized rats
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In urethane-anesthetized rats the intrathecal (i.t.) injection of 100 nmol anandamide produced a hypotensive effect (− 19.3 ± 1.6 mm Hg; n = 6) that was mimicked by i.t. administration of 0.25 nmol calcitonin gene-related peptide (CGRP; − 26.2 ± 1.8 mm Hg, n = 4). Both effects were antagonized either by the CGRP receptor antagonist CGRP_8–37 (5 nmol; i.t.) or by the γ-aminobutyric acid (GABA)_A receptor antagonist bicuculline (8.8 nmol, i.t) or by the GABA_B receptor antagonist 2-hydroxy saclofen (110 nmol; i.t.). On the contrary, blockade of spinal CGRP receptors by CGRP_8–37 did not modify the hypotensive response to either the GABA_A-receptor agonist muscimol (8.8 nmol; i.t.) or the GABA_B-receptor agonist baclofen (100 nmol; i.t). This result suggests a unidirectional effect of CGRP on the GABAergic system. The response to anandamide remained unaltered after acute inhibition of nitric oxide (NO) synthase activity by either i.t. (1 μmol) or i.v. (10 mg/kg) injection of N^G-nitro-l-arginine methyl ester (L-NAME), but increased significantly after long-term L-NAME administration (70 mg/kg/day; four weeks; p.o.), thus suggesting compensatory changes in cardiovascular homeostasis. It is proposed that the hypotensive effect of anandamide in urethane-anesthetized rats could involve the release of CGRP followed by the release of GABA in the spinal cord. NO does not appear to have a direct participation in the spinal mechanisms involved in the decrease of the blood pressure caused by anandamide.
Neurochemical properties of the middle cervical ganglion in the sheep
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The neurochemical properties of the ovine middle cervical ganglion (MCG) were studied using antibodies raised against tyrosine hydroxylase (TH), dopamine β-hydroxylase (DβH), neuropeptide Y (NPY), substance P (SP), calcitonin gene-related peptide (CGRP), vasoactive intestinal polypeptide (VIP) and galanin (GAL). Double-labelling immunocytochemistry revealed that the vast majority (95.5±0.8%) of postganglionic sympathetic MCG neurons expressed simultaneously both catecholamine-synthesizing enzymes (neurons were TH/DβH-positive). A large population of noradrenergic neurons exhibited immunoreactivity (IR) to NPY (62.2±2.2%), but single NPY-positive perikarya-lacking noradrenergic markers were also observed (2.0±0.3%). None of the examined MCG neuronal somata contained SP, CGRP, GAL or VIP. A moderate number of noradrenergic nerve fibres located amongst neuronal cell bodies was also found. In small number of these terminals the presence of NPY or GAL (but not CGRP or VIP) was detected. The ovine MCG was numerously innervated with SP-immunoreactive nerve fibres which sometimes formed basket-like formations around postganglionic neurons. The MCG exhibited a sparse CGRP-immunoreactive innervation and lacked VIP-positive nerve terminals. In many aspects the chemical coding of MCG postganglionic neurons and nerve terminals resembles that found in other mammalian cervico-thoracic paravertebral ganglia, but some important species-dependent differences exist. The functional implications of these differences remain to be elucidated.
The origin of sensory nerve fibers that innervate the submandibular salivary gland in the rat
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The origin of sensory nerves that innervate the submandibular salivary gland was investigated in the rat. After application of wheat germ agglutinin-horseradish peroxidase to the cut endings of the sympathetic and parasympathetic nerve branches at the hilus of the gland, labeled cells were mainly found in the dorsal root ganglia and the trigeminal ganglion, respectively. The labeled neurons in these ganglia were of various sizes compared to unlabeled neurons, suggesting that the sensory nerves of the gland conduct various modalities of sensory information.

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: This work was supported by a grant from the Ministry of Education.

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Calcitonin gene-related peptide containing sympathetic preganglionic and sensory neurons projecting to the superior cervical ganglion of the rat

Abstract

Brain Research

J. Auton. Nerv. Syst.

Neuroscience

Brain Research

Brain Research

Neuroscience

Brain Research

J. Auton. Nerv. Syst.

Brain Research

Brain Research

Brain Research

Brain Research