Innervation patterns of the middle cervical - stellate ganglion complex in the rat

doi:10.1016/0304-3940(90)90681-X

Neuroscience Letters

Volume 117, Issue 3, 18 September 1990, Pages 300-306

https://doi.org/10.1016/0304-3940(90)90681-X Get rights and content

Abstract

The present experiments were designed to clarify the distribution of innervation of the middle and inferior cervical ganglia in the rat (middle cervical-stellate ganglion complex), the sympathetic ganglia which give rise to virtually all cardiac sympathetic nerves. Seven or 28 days after middle cervical-stellate ganglionectomy (surgical sympathectomy) norepinephrine content was measured in 9 peripheral areas including both the left and right atria and ventricles of the heart. The results were also compared to chemical sympathectomy produced with 6-hydroxydopamine. Seven or 28 days after surgical sympathectomy norepinephrine concentrations were reduced in all cardiac regions by at least 94%. Norepinephrine concentration in sub-diaphragmatic (spleen), but not supra-diaphragmatic (left intrascapular fat, left forelimb muscle), non-cardiac organs was preserved at control levels. 6-Hydroxydopamine treatment significantly reduced the norepinephrine concentration in all of the cardiac and non-cardiac tissues. The present evidence indicates that the middle cervical-stellate ganglion complex in the rat projects to a rather limited number of peripheral organs. Additionally, surgical sympathectomy produces more selective cardiac sympathectomy than 6-hydroxydopamine.

References (15)

G. Jaim-Etcheverry et al.
Permanent depletion of peripheral norepinephrine in rats treated at birth with 6-hydroxydopamine
Eur. J. Pharmacol.
(1971)
W.C. Randall et al.
Intrapericardial denervation of the heart
J. Surg. Res.
(1980)
A.H. Anton et al.
A study of the factors affecting the aluminum oxide-trihydroxyindole procedure for the analysis of catecholamines
J. Pharmacol. Exp. Therap.
(1962)
D.W.J. Clark et al.
Long-lasting peripheral and central effects of 6-hydroxydopamine in rats
Br. J. Pharmacol.
(1972)
L.J. Felice et al.
Determination of catecholamines in rat brain parts by reverse-phase ion-pair liquid chromatography
J. Neurochem.
(1978)
L. Finch et al.
Rapid recovery of vascular adrenergic nerves in the rat after chemical sympathectomy with 6-hydroxydopamine
Br. J. Pharmacol.
(1973)
S.J. Fluharty et al.
Tyrosine hydroxylase activity in the sympathoadrenal system under basal and stressful conditions: effect of 6-hydroxydopamine
J. Pharmacol. Exp. Ther.
(1985)

There are more references available in the full text version of this article.

Cited by (35)

Interrogating autonomic peripheral nervous system neurons with viruses – A literature review
2020, Journal of Neuroscience Methods
Citation Excerpt :
Viral transneuronal tracing was used to identify the stellate ganglion cell groups that regulate the orthosympathetic outflow systems to the heart (Waldron et al., 2019). It is well known that the stellate ganglion is the principal source of postganglionic sympathetic efferent supply to the heart (Pardini et al., 1989, 1990; Farkas et al., 1998; Zhou et al., 2019). A schematic drawing of the peripheral autonomic innervation of the heart is provided in Fig. 2.
How rich functionality emerges from the rather invariant structural architecture of the peripheral autonomic nervous system remains one of the major mysteries in neuroscience. The high incidence of patients with neural circuit-related autonomic nervous system diseases highlights the importance of fundamental research, among others with neurotracing methods, into autonomic neuron functionality. Due to the emergence of neurotropic virus-based tracing techniques in recent years the access to neuronal connectivity in the peripheral autonomic nervous system has greatly been improved. This review is devoted to the anatomical distribution of neural circuits in the periphery of the autonomous nervous system and to the interaction between the autonomic nervous system and vital peripheral organs or tissues. The experimental evidence available at present has greatly expanded our understanding of autonomic peripheral nervous system neurons.
Ageing, the autonomic nervous system and arrhythmia: From brain to heart
2018, Ageing Research Reviews
Citation Excerpt :
The preganglionic axons then terminate in either paravertebral (cervical, thoracic, lumbar and sacral) or prevertebral (celiac, superior mesenteric and inferior mesenteric) ganglia (Armour, 2010). The cell bodies of postganglionic sympathetic neurons associated with the cardiac ANS primarily reside in the paravertebral stellate ganglia (C7-8 to T1-2) and the axons terminate on the myocardium as the superior, middle and inferior cardiac nerves (Kawashima, 2005; Pardini et al., 1989, 1990; Shen and Zipes, 2014). In the sympathetic system, the main neurotransmitter of preganglionic axons is acetylcholine and the main neurotransmitter of postganglionic axons is norepinephrine.
An ageing myocardium possesses significant electrophysiological alterations that predisposes the elderly patient to arrhythmic risk. Whilst these alterations are intrinsic to the cardiac myocytes, they are modulated by the cardiac autonomic nervous system (ANS) and consequently, ageing of the cardiac ANS is fundamental to the development of arrhythmias. A systems-based approach that incorporates the influence of the cardiac ANS could lead to better mechanistic understanding of how arrhythmogenic triggers and substrates interact spatially and temporally to produce sustained arrhythmia and why its incidence increases with age. Despite the existence of physiological oscillations of ANS activity on the heart, pathological oscillations can lead to defective activation and recovery properties of the myocardium. Such changes can be attributable to the decrease in functionality and structural alterations to ANS specific receptors in the myocardium with age. These altered ANS adaptive responses can occur either as a normal ageing process or accelerated in the presence of specific cardiac pathologies, such as genetic mutations or neurodegenerative conditions. Targeted intervention that seek to manipulate the ageing ANS influence on the myocardium may prove to be an efficacious approach for the management of arrhythmia in the ageing population.
Sympathetic nervous remodeling is induced in the intermediolateral nucleus after myocardial infarction – Role of BDNF-TrkB axis-
2018, Neuroscience Letters
Citation Excerpt :
These results support our hypothesis that activation of the BDNF-TrkB axis is associated with sympathetic nervous remodeling of the IML after MI. Several studies have shown that neural remodeling of SG is induced after MI [1–6]. In contrast, little is known about the neural remodeling at the upper level of the SNS for the heart.
Several studies have shown that neural remodeling in stellate ganglia (SG) is induced by myocardial infarction (MI). It remains unclear whether neural remodeling after MI is limited in SG within the sympathetic nervous system (SNS). MI was induced in a rat model by ligation of the left anterior descending artery. Neural remodeling in the intermediolateral nucleus (IML) and SG was assessed by immunohistochemistry 2 weeks after MI. The mRNA and protein expressions of brain-derived neurotrophic factor (BDNF), tropomyosin-related kinase receptor (TrkB) and extracellular signal-regulated kinase (ERK) were measured by quantitative RT-PCR, immunohistochemistry and Western blotting 1 week after MI. The neuronal size and axonal density of IML were increased after MI compared to sham. The density of growth-associated protein-43, a protein upregulated in axons undergoing nerve sprouting, was increased after MI compared to sham. The fluorescence intensity of BDNF and TrkB in IML were significantly higher in the MI group than in the sham group. In addition, mRNA expressions of BDNF and TrkB in the spinal cord at the Th2 level was increased after MI. Finally, the percentage of phospho-ERK-immunoreactive cells in IML was significantly higher in the MI group than in the sham group. In conclusion, neural remodeling after MI in IML is associated with the activation of BDNF-TrkB axis. Morphological remodeling throughout the SNS may be involved in sustained activation of sympathetic tone after MI.
Differential expression of tyrosine hydroxylase and transporters in the right and left stellate ganglion of socially isolated rats
2014, Autonomic Neuroscience: Basic and Clinical
Chronic isolation stress of adult rat males acted increasing gene expression of tyrosine hydroxylase (TH) and neuronal norepinephrine transporter (NET) in the right stellate ganglia, while vesicular monoamine transporter 2 (VMAT2) level remained unchanged. The stress decreased protein level of TH, as well as mRNA levels for NET and VMAT2 in the left stellate ganglia, but expressed no effect on protein levels of these two transporters. These results demonstrate asymmetry in noradrenegic genes in the right and left stellate ganglia during stress and provide molecular evidence to help explain the difference in response to the stress.
Protein malnutrition modifies medullary neuronal recruitment in response to intermittent stimulation of the baroreflex
2012, Brain Research
Citation Excerpt :
Ventromedial medullary region is described to group neurons that govern the sympathetic outflow to the heart and thermogenesis (Cao and Morrison, 2003; Morrison and Nakamura, 2011; Morrison et al., 2012; Salo et al., 2009). Anatomic and functional studies showed marked labeling in RVMM (Amendt et al., 1979; Chiba and Masuko, 1989; Hofstetter et al., 2005; Loewy, 1981; Morrison, 1993; Pardini et al., 1990). Unlike the baseline tonic and phasic activities of RVLM (Campos and McAllen, 1997; Campos and McAllen, 1999a; Campos and McAllen, 1999b), stimulation of RVMM neurons produces pronounced tachycardia (Cao and Morrison, 2003; Cao and Morrison, 2006; Morrison, 2003).
Protein malnutrition after weaning changes the neurotransmission in neural pathways that organize cardiovascular reflexes in rats. The present study evaluates whether protein malnutrition alters the expression of c-fos protein (immediate-early gene expression) in central areas involved in the control of cardiovascular reflexes after intermittent stimulation of the baroreflex. The main nuclei we focused were paraventricular hypothalamus (PVH); nucleus tract solitarii (NTS); rostral ventromedial medulla (RVMM); rostral (RVLM) and caudal ventrolateral medulla (CVLM). Male Fisher rats at 28 days were submitted to two different isocaloric diets during the subsequent 35 days: control (CT) (15% protein) and malnourished (MN) (6% protein). thirty min of intermittent (every 3 min) baroreflex stimulation was performed by infusing phenylephrine (Phe—0.25 mM) or, as control, 0.9% NaCl (Sal). Following ninety minutes, animals were anesthetized and perfused. The removed brains were sectioned (35 μm) and used for c-fos immunohistochemistry. Images were analyzed using the software Leica Q Win. Despite not altering the baseline MAP, malnutrition increased baseline HR and expression of c-fos in RVMM. Increases in c-fos expression after intermittent stimulation of baroreflex were evident in the PVH, medial NTS and CVLM in both dietary protocols. Current data further revealed a differential neuronal recruitment to stimulation of baroreflex in the caudal commissural and rostral NTS and RVLM of MN. We conclude that protein malnutrition modifies the cardiovascular control and the pattern of central response to baroreflex stimulation.
Psychosocial stress-related changes in gene expression of norepinephrine biosynthetic enzymes in stellate ganglia of adult rats
2009, Autonomic Neuroscience: Basic and Clinical
In this study we investigated the changes in norepinephrine biosynthetic enzymes tyrosine hydroxylase (TH), dopamine β-hydroxylase (DBH) and phenylethanolamine N-methyltransferase (PNMT) gene expression in the stellate ganglia of naive controls and long-term socially isolated (12 weeks) adult rats and the response of these animals to additional immobilization stress. Psychosocial stress produced a significant increase of both TH mRNA and DBH mRNA levels in stellate ganglia. Additional immobilization of long-term psychosocially stressed rats expressed no effect on gene expression of these enzymes. The results presented here suggest that psychosocial stress-induced increase in gene expression of norepinephrine biosynthetic enzymes in stellate ganglia may be connected to the increased risk of cardiovascular disease.

View all citing articles on Scopus

^☆: This research was supported by grants from the Department of Veterans Affairs. NIH National Heart, Lung, and Blood Institute (HL 38137), and the Iowa Affiliate of the American Heart Association.

View full text

Innervation patterns of the middle cervical - stellate ganglion complex in the rat☆

Abstract

Eur. J. Pharmacol.

J. Surg. Res.

A study of the factors affecting the aluminum oxide-trihydroxyindole procedure for the analysis of catecholamines

J. Pharmacol. Exp. Therap.

Long-lasting peripheral and central effects of 6-hydroxydopamine in rats

Br. J. Pharmacol.

Determination of catecholamines in rat brain parts by reverse-phase ion-pair liquid chromatography

J. Neurochem.

Rapid recovery of vascular adrenergic nerves in the rat after chemical sympathectomy with 6-hydroxydopamine

Br. J. Pharmacol.

Tyrosine hydroxylase activity in the sympathoadrenal system under basal and stressful conditions: effect of 6-hydroxydopamine

J. Pharmacol. Exp. Ther.