Sympathetic neurons in lower cervical ganglia send axons through the superior cervical ganglion

doi:10.1016/0306-4522(81)90213-X

Neuroscience

Volume 6, Issue 9, September 1981, Pages 1783-1791

https://doi.org/10.1016/0306-4522(81)90213-X Get rights and content

Abstract

In addition to the preganglionic axons which innervate the superior cervical ganglia, the cervical sympathetic trunks of the rat have been shown to contain axons of ganglionic neurons. Following the application of horseradish peroxidase to the cut cervical sympathetic trunk just caudal to the superior cervical ganglion, a population of approximately 300 labeled neurons was found in the inferior and middle cervical ganglia. The labeled neurons were localized primarily in the more rostral regions of these ganglia. The axons of most of these neurons entered the superior cervical ganglion, passed through it, and left via the external carotid nerve.

The relevance of these observations to physiological studies on the cervical sympathetic nervous system is discussed

Reference (34)

AguayoA.J. et al.
Spontanteous loss of axons in sympathetic unmyelinated nerve fibers of the rat during development
Brain Res.
(1973)
WimerC.
A method for estimating nuclear diameter to correct for split nuclei in neuronal counts
Brain Res.
(1977)
AbercrombieM.
Estimation of nuclear population from microtome sections
Anat. Rec.
(1946)
BlackmanJ.G. et al.
Intracellular recordings from ganglia of the thoracic sympathetic chain of the guinea-pig
J. Physiol.
(1969)
BowersC.W. et al.
Localization of neurons in the rat superior cervical ganglion that project into different post-ganglionic trunks
J. Comp. Neurol.
(1979)
Brooks-FournierR. et al.
The ratio of preganglionic axons to postganglionic cells in the sympathetic nervous system
Soc. Neurosci. Abstr.
(1979)
BulbringE.
The action of adrenaline on transmission in the superior cervical ganglion
J. Physiol.
(1944)
CeccarelliB. et al.
Adrenergic reinnervation of smooth muscle of nictitating membrane by preganglionic sympathetic fibres
J. Physiol.
(1972)
DouglasW.W. et al.
On the excitant effect of acetylcholine on structures in the preganglionic trunk of the cervical sympathetic: with a note on the anatomical complexities of the region
J. Physiol.
(1960)
DouglasW.W. et al.
The conduction of impulses through the superior cervical and accessory cervical ganglia of the rabbit
J. Physiol.
(1956)

DunN. et al.

The presynaptic site of action of norepinephrine in the superior cervical ganglion of guinea pig

J. Pharmacol. Exp. Therap.

(1977)

DyckP.J. et al.

Electron microscopic observations on degeneration and regeneration of unmyelinated fibers

Brain

(1972)

FoleyJ.O.

The components of the cervical sympathetic trunk with special reference to its accessory cells and ganglia

J. Comp. Neurol.

(1945)

FoleyJ.O. et al.

A quantitative and experimental study of the cervical sympathetic trunk

J Comp. Neurol.

(1940)

GreeneE.C.

Anatomy of the rat

HedgerJ.H. et al.

Anatomical study of the cervical sympathetic trunk and ganglia in the albino rat

Acta. Anal.

(1976)

HendryI.A. et al.

Morphometric analysis of rat superior cervical ganglion after axotomy and nerve growth factor treatment

J. Neurocyt.

(1976)

Cited by (34)

Stereological and allometric studies on neurons and axo-dendritic synapses in superior cervical ganglia
2014, International Review of Cell and Molecular Biology
Citation Excerpt :
In the upper thoracic chain segment, they are mainly ascending (cranially directed) and in the cervical sympathetic trunk—where SCG is inserted—all the preganglionic fibers are directed cranially. In this trunk, however, there are also caudally directed postganglionic fibers, originating in the SCG, and cranially directed postganglionic fibers, originating in the middle and lower cervical ganglia (Bowers and Zigmond, 1981). In the rat, unlike other species, such as humans and cats, the great majority of preganglionic fibers are unmyelinated.
The superior cervical ganglion (SCG) plays an important role in neuropathies including Horner's syndrome, stroke, and epilepsy. While mammalian SCGs seem to share certain organizational features, they display natural differences related to the animal size and side and the complexity and synaptic coverage of their dendritic arborizations. However, apart from the rat SCG, there is little information concerning the number of SCG neurons and synapses, and the nature of relationships between body weight and the numbers and sizes of neurons and synapses remain uncertain. In the recognition of this gap in the literature, in this chapter, we reviewed the current knowledge on the SCG structure and its remodeling during postnatal development across a plethora of large mammalian species, focusing on exotic rodents and domestic animals. Instrumentally, we present stereology as a state-of-the-art 3D technology to assess the SCG 3D structure unbiasedly and suggest future research directions on this topic.
Induction of zinc-finger proliferation 1 expression in non-myelinating Schwann cells after denervation
2008, Neuroscience
Citation Excerpt :
Using the same antibody we showed that tSCs also express Zipro1 and that its levels increased there after denervation as well. Neuronal cell bodies that extend into the caudal segments of the rat CST have been previously reported (Bowers and Zigmond, 1981). The fact that CST neurons are Zipro1+ is not surprising as granule cells in the cerebellum and other regions of the brain have been reported to be Zipro1+ by in situ hybridization by others (Yang et al., 1996) and ourselves (Fig. 2 and data not shown).
Terminal Schwann cells (tSCs) are non-myelinating glia that wrap the nerve terminal at the neuromuscular junction. They are required for the maintenance of the neuromuscular synapse and are likely to play essential roles in the restoration of synaptic connections after nerve injury. tSCs acquire a reactive phenotype after nerve damage characterized by the extension of cellular processes that may facilitate reinnervation. The molecular signaling events underpinning the tSC reactive state remain elusive, in particular, little is known about transcription factors involved in the transcriptional reprogramming during tSC activation. Prior research implicated nine members of the zinc-finger transcription factor family in Schwann cell (SC) development and myelination, and levels of one such protein were reported increased in other non-myelinating SCs after denervation. We hypothesize that zinc-finger transcription factors could play a role during tSC activation. Because of their relative paucity, tSCs are difficult to study molecularly. Here, we used the rat cervical sympathetic trunk (CST), an autonomic nerve in which non-myelinating SCs are the predominant cell type, to isolate zinc-finger protein (ZFP) cDNAs by reverse transcriptase–polymerase chain reaction. We isolated 29 unique ZFP sequences of which zinc proliferation 1 (Zipro1) was the most abundant. We found that after CST transection, levels for Zipro1 mRNA doubled and that Zipro1 protein expression increased in non-myelinating CST SCs. We also determined that Zipro1 is expressed in tSCs and its levels increased following skeletal muscle denervation. Thus, Zipro1 is a good candidate for a transcription factor involved in activation of non-myelinating SCs in general, and tSCs in particular.
Activating transcription factor 3 immunoreactivity identifies small populations of axotomized neurons in rat cervical sympathetic ganglia after transection of the preganglionic cervical sympathetic trunk
2007, Brain Research
Citation Excerpt :
In addition, we previously showed that two populations of postganglionic neurons project into this trunk. One of these is a small group of neurons whose cell bodies are located primarily in the caudal part of the SCG (Bowers and Zigmond, 1979), and the other is a group of neurons whose cell bodies are located primarily in the rostral portions of the middle and inferior cervical ganglia (MICG; Bowers and Zigmond, 1981). Transection of the CST near the SCG, thus, produces a proximal axotomy to certain neurons in the SCG, while producing a distal axotomy to certain neurons in the MICG.
Activating transcription factor 3 (ATF3) has been proposed as a marker for injured neurons. Thus, while undetectable normally in sensory, motor, or sympathetic neurons, ATF3-like immunoreactivity (ATF3-IR) is readily detectable in such cells after axotomy. Here we examined ATF3-IR in the superior cervical ganglion (SCG) and the middle and inferior cervical ganglia (MICG) after transection of the predominantly preganglionic cervical sympathetic trunk (CST). The purpose of the study was to determine whether neurons in the SCG would exhibit ATF3-IR after decentralization and, if they did not, whether the induction of ATF3-IR was sensitive enough to identify the small numbers of neurons in the SCG and MICG that project their axons into the CST. Following transection of the CST, the majority of deafferented neurons in the SCG showed no ATF3-IR; however, a small group of neurons in both the SCG and MICG were labeled, and the location of the labeled neurons within these ganglia corresponded to that of neurons axotomized by this procedure. Furthermore, the ATF3-positive neurons in the MICG could be retrogradely labeled from the transected CST. In addition, a large number of smaller cells were labeled in the SCG, though not in the MICG, and some of these cells were double labeled with an antiserum to the glial protein S-100. These data indicate that, after transection of the CST, neuronal labeling in the SCG and MICG is restricted to axotomized neurons but that in addition there is extensive labeling of glial cells associated with anterograde degeneration within the SCG.
Autonomic neural signals in bone: Physiological implications for mandible and dental growth
2004, Life Sciences
Signals derived from the autonomic nervous system exert potent effects on osteoclast and osteoblast function. A ubiquitous sympathetic and sensory innervation of all periosteal surfaces exists and its disruption affects bone remodeling. Several neuropeptides, neurohormones and neurotransmitters and their receptors are detectable in bone. Bone mineral content decreased in sympathetically denervated mandibular bone. When a mechanical stress was superimposed on mandibular bone by cutting out the lower incisors, an increase in bone density ensued providing the sympathetic innervation was intact. A lower eruption rate of sympathetically denervated incisors at the impeded eruption side, and a higher eruption rate of denervated incisors at the unimpeded side were also observed. A normal sympathetic neural activity appears to be a pre-requisite for maintaining a minimal normal unimpeded incisor eruption and for keeping the unimpeded eruption to attain abnormally high velocities under conditions of stimulated incisor growth. These and other results suggest that the sympathetic nervous system plays an important role in mandibular bone metabolism.
Autonomic Nervous System
2004, The Rat Nervous System
Small intensely fluorescent cells of the rat paracervical ganglion synthesize adrenaline, receive afferent innervation from postganglionic cholinergic neurones, and contain muscarinic receptors
1999, Brain Research
In the paracervical ganglion (PCG) of the rat, double-labelling immunofluorescence for catecholamine-synthesizing enzymes and HPLC measurement of catecholamine contents were first performed to evaluate whether intraganglionic small intensely fluorescent (SIF) cells are capable of synthesizing adrenaline. Immunolabelling for tyrosine hydroxylase (TH), dopamine β-hydroxylase and phenylethanolamine-N-methyl transferase (PNMT) occurred in all SIF cells of the PCG, thus demonstrating the presence of all the enzymes required for adrenaline biosynthesis. Adrenaline levels were undetectable in the PCG but to test the hypothesis that PNMT is active in SIF cells, catecholamines were measured in ganglia of rats pretreated with pargyline, an inhibitor of the monoamine oxidase, the major enzyme involved in the catecholamine degradation. Pargyline treatment increased adrenaline levels in the PCG, thus demonstrating that SIF cells are capable of adrenaline synthesis. The undetectable levels of adrenaline in the PCG of untreated rats suggested a slow rate of biosynthesis of adrenaline in the ganglion. Furthermore, the use of double-labelling showed that SIF cells of the PCG were stained for muscarinic receptors and were approached by varicose ChAT-immunoreactive nerve fibres. Nerve fibres immunoreactive for ChAT were also observed associated with nerve cell bodies of ganglion neurones. Following deafferentation of the PCG, the ChAT-immunoreactive nerve fibres surrounding nerve cell bodies totally disappeared indicating their preganglionic origin, while those associated with SIF cells did not degenerate, which demonstrate that they derived from intraganglionic cholinergic neurones. Taken together, the results show that adrenaline may be a transmitter for SIF cells in the PCG and suggest that cholinergic neurones of the parasympathetic division of the PCG can modulate the SIF cell activity through the activation of muscarinic receptors.

View all citing articles on Scopus

View full text

Sympathetic neurons in lower cervical ganglia send axons through the superior cervical ganglion

Abstract

Brain Res.

Brain Res.

Estimation of nuclear population from microtome sections

Anat. Rec.

Intracellular recordings from ganglia of the thoracic sympathetic chain of the guinea-pig

J. Physiol.

Localization of neurons in the rat superior cervical ganglion that project into different post-ganglionic trunks

J. Comp. Neurol.

The ratio of preganglionic axons to postganglionic cells in the sympathetic nervous system

Soc. Neurosci. Abstr.

The action of adrenaline on transmission in the superior cervical ganglion

J. Physiol.

Adrenergic reinnervation of smooth muscle of nictitating membrane by preganglionic sympathetic fibres

J. Physiol.

On the excitant effect of acetylcholine on structures in the preganglionic trunk of the cervical sympathetic: with a note on the anatomical complexities of the region

J. Physiol.

The conduction of impulses through the superior cervical and accessory cervical ganglia of the rabbit

J. Physiol.

The presynaptic site of action of norepinephrine in the superior cervical ganglion of guinea pig

J. Pharmacol. Exp. Therap.

Electron microscopic observations on degeneration and regeneration of unmyelinated fibers

Brain

The components of the cervical sympathetic trunk with special reference to its accessory cells and ganglia

J. Comp. Neurol.

A quantitative and experimental study of the cervical sympathetic trunk

J Comp. Neurol.

Anatomy of the rat

Anatomical study of the cervical sympathetic trunk and ganglia in the albino rat

Acta. Anal.

Morphometric analysis of rat superior cervical ganglion after axotomy and nerve growth factor treatment

J. Neurocyt.