Unusual Autonomic Ganglia: Connections, Chemistry, and Plasticity of Pelvic Ganglia

doi:10.1016/S0074-7696(08)61778-7

International Review of Cytology

Volume 193, 1999, Pages 1-69

https://doi.org/10.1016/S0074-7696(08)61778-7 Get rights and content

The pelvic ganglia provide the majority of the autonomic nerve supply to reproductive organs, urinary bladder, and lower bowel. Of all autonomic ganglia, they are probably the least understood because in many species their anatomy is particularly complex. Furthermore, they are unusual autonomic ganglia in many ways, including their connections, structure, chemistry, and hormone sensitivity. This review will compare and contrast the normal structure and function of pelvic ganglia with other types of autonomic ganglia (sympathetic, parasympathetic, and enteric). Two aspects of plasticity in the pelvic pathways will also be discussed. First, the influence of gonadal steroids on the maturation and maintenance of pelvic reflex circuits will be considered. Second, the consequences of nerve injury will be discussed, particularly in the context of the pelvic ganglia receiving distributed spinal inputs. The review demonstrates that in many ways the pelvic ganglia differ substantially from other autonomic ganglia. Pelvic ganglia may also provide a useful system in which to study many fundamental neurobiological questions of broader relevance.

References (369)

T. Akasu et al.
Synaptic transmission and function of parasympathetic ganglia
Prog. Neurobiol.
(1995)
T. Akasu et al.
Evidence for a catecholamine-mediated slow hyperpolarizing synaptic response in parasympathetic ganglia
Brain Res.
(1986)
P. Alm
On the autonomic innervation of the human vas deferens
Brain Res. Bull.
(1982)
P. Alm et al.
Histochemical demonstration of a concomitant reduction in neural vasoactive intestinal polypeptide, acetylcholinesterase, and noradrenaline of cat uterus during pregnancy
Neuroscience
(1986)
H.A. Baker et al.
Histochemical and biochemical characterization of the rat paracervical ganglion
Brain Res.
(1977)
R. Baron et al.
Neurons projecting rostrally in the hypogastric nerve of the cat
J. Auton. Nervous System
(1988)
M. Bitran et al.
Age and castration modulate the inhibitory action of neuropeptide Y on neurotransmission in the rat vas deferens
Eur. J. Pharmacol.
(1991)
A.M. Booth et al.
A study of facilitation in vesical parasympathetic ganglia of the cat using intracellular recording techniques
Brain Res.
(1979)
J.A. Brock et al.
Impulse conduction in sympathetic nerve terminals in the guinea-pig vas deferens and the role of the pelvic ganglia
Neuroscience
(1992)
M. Costa et al.
Projections of substance P-containing neurons within the guinea-pig small intestine
Neuroscience
(1981)

M. Costa et al.

Chemical coding of enteric neurons

Prog. Brain Res.

(1986)

R. Crowe et al.

Intramural neurones of the guinea-pig urinary bladder: Histochemical localization of putative neurotransmitters in cultures and newborn animals

J. Auton. Nervous System

(1986)

W.G. Dail et al.

Composition of the pelvic nerve

Exp. Neurol.

(1986)

W.G. Dail et al.

Localization of vasoactive intestinal polypeptide in penile erectile tissue and in the major pelvic ganglion of the rat

Neuroscience

(1983)

W.G. Dail et al.

The hypogastric nerve innervates a population of penile neurons in the pelvic plexus

Neuroscience

(1985)

W.G. Dail et al.

The hypogastric nerve pathway to penile erectile tissue: Histochemical evidence supporting a vasodilator role

J. Auton. Nervous System

(1986)

F. de Castro et al.

Effects of postganglionic nerve section on synaptic transmission in the superior cervical ganglion of the guinea-pig

Neuroscience

(1995)

W.C. de Groat et al.

Organization of the sacral parasympathetic reflex pathways to the urinary bladder and large intestine

J. Auton. Nervous System

(1981)

Y.-Q. Ding et al.

The major pelvic ganglion is the main source of nitric oxide synthase-containing nerve fibers in penile erectile tissue of the rat

Neurosci. Lett.

(1993)

J.S. Dixon et al.

Neuropeptide studies on the human vas deferens

J. Auton. Nervous System

(1991)

D.J. Adams et al.

Electrophysiological properties of autonomic ganglion neurons

T. Akasu et al.

Adenosine mediates a slow hyperpolarizing synaptic potential in autonomic neurones

Nature

(1984)

P. Alm et al.

Co-existence and origin of peptidergic and adrenergic nerves in the guinea pig uterus. Retrograde tracing and immunocytochemistry, effects of chemical sympathectomy, capsaicin treatment and pregnancy

Cell Tissue Res.

(1988)

G.F. Andersson et al.

The response of autonomic receptors to castration and testosterone in the urinary bladder of the rabbit

J. Urol.

(1988)

K.-E. Andersson

Pharmacology of lower urinary tract smooth muscles and penile erectile tissues

Pharmacol. Rev.

(1993)

K.-E. Andersson et al.

Physiology of penile erection

Physiol. Rev.

(1995)

K.E. Andersson et al.

Castration enhances NANC nerve-mediated relaxation in rabbit isolated corpus cavernosum

Acta Physiol. Scand.

(1992)

P.-O. Andersson et al.

Colonic motor and vascular responses to pelvic nerve stimulation and their relation to local peptide release in the cat

J. Physiol.

(1983)

A.P. Arnold et al.

Gonadal steroid induction of structural sex differences in the central nervous system

Annu. Rev. Neurosci.

(1984)

U. Arvidsson et al.

Vesicular acetylcholine transporter (VAChT) protein: A novel and unique marker for cholinergic neurons in the central and peripheral nervous systems

J. Comp. Neurol.

(1997)

B. Baljet et al.

The extrinsic innervation of the abdominal organs of the female rat

Acta Anat.

(1979)

B. Baljet et al.

The extrinsic innervation of the pelvic organs in the female rat

Anat. Rec.

(1980)

P. Baluk

Structure of autonomic ganglia

H. Banns et al.

Recovery of choline acetyltransferase activity in the rat urinary bladder deprived of half of its innervation

Acta Physiol. Scand.

(1980)

R. Baron et al.

Afferent and sympathetic neurons projecting into the lumbar visceral nerves of the male rat

J. Comp. Neurol.

(1991)

R. Baron et al.

The afferent and sympathetic components of the lumbar spinal outflow to the colon and pelvic organs in the cat. III. The colonic nerves, incorporating an analysis of all components of the lumbar prevertebral outflow

J. Comp. Neurol.

(1985)

R. Baron et al.

The afferent and sympathetic components of the lumbar spinal outflow to the colon and pelvic organs in the cat. I. The hypogastric nerve

J. Comp. Neurol.

(1985)

K. Becker

Paraganglienzellen in Ganglion cervicale uteri der Maus

Z. Zeitschrift.

(1972)

C. Bell et al.

Observations on the loss of catecholamine fluorescence from intrauterine adrenergic nerves during pregnancy in the guinea-pig

J. Reprod. Fertil.

(1978)

C. Bell et al.

Localisation of norepinephrine and acetylcholinesterase in separate neurons supplying the guinea-pig vas deferens

J. Pharmacol. Exp. Ther.

(1967)

O. Belluzzi et al.

Identification of delayed potassium and calcium current in the rat sympathetic neuron under voltage-clamp conditions

J. Physiol.

(1985)

H.-R. Berthoud et al.

Simultaneous labeling of vagal innervation of the gut and afferent projections from the visceral forebrain with DiI injected into the dorsal vagal complex in the rat

J. Comp. Neurol.

(1990)

H.-R. Berthoud et al.

Topography of efferent vagal innervation of the rat gastrointestinal tract

Am. J. Physiol.

(1991)

J.G. Blackman et al.

Transmission from preganglionic fibres in the hypogastric nerve to peripheral ganglia of male guinea-pigs

J. Physiol.

(1969)

H.D. Boyd et al.

Three electrophysiological classes of guinea pig sympathetic neurone have distinct morphologies

J. Comp. Neurol.

(1996)

A.F. Brading et al.

Electrical and mechanical responses of guinea-pig bladder muscle to nerve stimulation

Br. J. Pharmacol.

(1989)

M.M. Brauer et al.

Postnatal development of noradrenaline-containing nerves of the rat uterus

J. Auton. Nervous System

(1992)

S.M. Breedlove

Sexual dimorphism in the vertebrate nervous system

J. Neurosci.

(1992)

A. Broberg et al.

Consequence of neonatal androgenization and castration for future levels of norepinephrine transmitter in uterus and vas deferens of the rat

Neuroendocrinology

(1974)

G. Burnstock

The purinergic nerve hypothesis

Ciba Foundation Symp.

(1977)

Cited by (97)

Spatiotemporal mapping of sensory and motor innervation of the embryonic and postnatal mouse urinary bladder
2021, Developmental Biology
Citation Excerpt :
We extended this component of the study through the postnatal period and compared with adult innervation patterns, in both male and female mice. The majority of autonomic axons in the bladder originate from neuronal cell bodies located in the pelvic ganglion (PG), also known in rodents as the major pelvic ganglion or, in humans, the inferior hypogastric plexus (Ernsberger et al., 2020; Keast, 1999). This mixed sympathetic-parasympathetic ganglion comprises a mixture of noradrenergic and cholinergic neurons, each with spinal inputs from distinct regions.
The primary function of the urinary bladder is to store urine (continence) until a suitable time for voiding (micturition). These distinct processes are determined by the coordinated activation of sensory and motor components of the nervous system, which matures to enable voluntary control at the time of weaning. Our aim was to define the development and maturation of the nerve-organ interface of the mouse urinary bladder by mapping the organ and tissue distribution of major classes of autonomic (motor) and sensory axons. Innervation of the bladder was evident from E13 and progressed dorsoventrally. Increasing defasciculation of axon bundles to single axons within the muscle occurred through the prenatal period, and in several classes of axons underwent further maturation until P7. Urothelial innervation occurred more slowly than muscle innervation and showed a clear regional difference, from E18 the bladder neck having the highest density of urothelial nerves. These features of innervation were similar in males and females but varied in timing and tissue density between different axon classes. We also analysed the pelvic ganglion, the major source of motor axons that innervate the lower urinary tract and other pelvic organs. Cholinergic, nitrergic (subset of cholinergic) and noradrenergic neuronal cell bodies were present prior to visualization of these axon classes within the bladder. Examination of cholinergic structures within the pelvic ganglion indicated that connections from spinal preganglionic neurons to pelvic ganglion neurons were already present by E12, a time at which these autonomic ganglion neurons had not yet innervated the bladder. These putative preganglionic inputs increased in density prior to birth as axon terminal fields continued to expand within the bladder tissues. Our studies also revealed in numerous pelvic ganglion neurons an unexpected transient expression of calcitonin gene-related peptide, a peptide commonly used to visualise the peptidergic class of visceral sensory axons. Together, our outcomes enhance our understanding of neural regulatory elements in the lower urinary tract during development and provide a foundation for studies of plasticity and regenerative capacity in the adult system.
Spinal cord injury leads to atrophy in pelvic ganglia neurons
2020, Experimental Neurology
Among the most devastating sequelae of spinal cord injury (SCI) are genitourinary and gastrointestinal dysfunctions. Post-ganglionic neurons in pelvic ganglia (PG) directly innervate and regulate the function of the lower urinary tract (LUT), bowel, and sexual organs. A better understanding of how SCI affects PG neurons is essential to develop therapeutic strategies for devastating gastrointestinal and genitourinary complications ensuing after injury. To evaluate the impact of SCI on the morphology of PG neurons, we used a well- characterized rat model of upper thoracic SCI (T3 transection) that causes severe autonomic dysfunction. Using immunohistochemistry for neuronal markers, the neuronal profile size frequency distribution was quantified at one-, four-, and eight-weeks post SCI using recursive translation. Our investigation revealed an SCI-dependent leftward shift in neuronal size (i.e. atrophy), observable as early as one-week post injury. However, this effect was more pronounced at four and eight-weeks post-SCI. These findings demonstrate the first characterization of SCI-associated temporal changes in morphology of PG neurons and warrant further investigation to facilitate development of therapeutic strategies for recovery of autonomic functions following SCI.
Autonomic nervous system and male reproduction
2018, Encyclopedia of Reproduction
The autonomic nervous system regulates the smooth muscle activity, glandular secretions and blood flow in the male reproductive organs and so is essential for erection, emission and ejaculation. The onset, intensity, duration and coordination of these events also depend on sensory, brain and spinal circuits. In this chapter, general principles of autonomic regulation are followed by more detailed discussion of how neural activity affects different reproductive organs, the impact of sex hormones on this neural communication and relevance to several clinical conditions.
Neurophysiologic Mechanisms of Human Large Intestinal Motility
2018, Physiology of the Gastrointestinal Tract, Sixth Edition
The human colon absorbs water and electrolytes stores feces until elimination is socially convenient, and salvages nutrients by bacterial metabolism of nutrients that were not absorbed in the small intestine. Colonic motility is characterized by patterned contractions of longitudinal and circular muscle layers, which result from interactions between several types of cells in the gut wall (neurons, glia, interstitial cells of Cajal, smooth muscle cells, enteroendocrine cells, resident white blood cells, and fibroblast-like cells) and which are regulated by the extrinsic nervous system. Motility is closely integrated with colonic secretion and absorption. This chapter reviews colonic motility and where possible, relates anatomy, coordinated motor patterns, and propulsion of material to their underlying cellular and molecular mechanisms. Since there are considerable interspecies differences in colonic anatomy and function, the emphasis is on colonic sensorimotor functions in health and disease in humans, supplemented by data from other species, where necessary.
Insights into the background of autonomic medicine
2017, Revista Portuguesa de Cardiologia
Knowledge of the physiology underlying the autonomic nervous system is pivotal for understanding autonomic dysfunction in clinical practice. Autonomic dysfunction may result from primary modifications of the autonomic nervous system or be secondary to a wide range of diseases that cause severe morbidity and mortality. Together with a detailed history and physical examination, laboratory assessment of autonomic function is essential for the analysis of various clinical conditions and the establishment of effective, personalized and precise therapeutic schemes. This review summarizes the main aspects of autonomic medicine that constitute the background of cardiovascular autonomic dysfunction.
O conhecimento subjacente à fisiologia do sistema nervoso autónomo é fundamental para se entender a disfunção autonómica na prática clinica. A disfunção autonómica pode resultar primariamente de modificações do sistema ou, secundariamente, a uma série de patologias conducentes a morbilidade ou mortalidade. Juntamente com a colheita detalhada da história clínica e do exame objetivo, a avaliação autonómica laboratorial torna-se essencial na análise de algumas condições clínicas e no estabelecimento de esquemas terapêuticos mais eficazes, refinados e personalizados. Assim, nesta revisão sumarizam-se os aspetos mais relevantes da fisiologia autonómica subjacente a disfunção autonómica cardiovascular.
Renaming all spinal autonomic outflows as sympathetic is a mistake
2017, Autonomic Neuroscience: Basic and Clinical

View all citing articles on Scopus

View full text

Unusual Autonomic Ganglia: Connections, Chemistry, and Plasticity of Pelvic Ganglia

Prog. Neurobiol.

Brain Res.

Brain Res. Bull.

Neuroscience

Brain Res.

J. Auton. Nervous System

Eur. J. Pharmacol.

Brain Res.

Neuroscience

Neuroscience

Prog. Brain Res.

J. Auton. Nervous System

Exp. Neurol.

Neuroscience

Neuroscience

J. Auton. Nervous System

Neuroscience

J. Auton. Nervous System

Neurosci. Lett.

J. Auton. Nervous System

Electrophysiological properties of autonomic ganglion neurons

Adenosine mediates a slow hyperpolarizing synaptic potential in autonomic neurones

Nature

Co-existence and origin of peptidergic and adrenergic nerves in the guinea pig uterus. Retrograde tracing and immunocytochemistry, effects of chemical sympathectomy, capsaicin treatment and pregnancy

Cell Tissue Res.

The response of autonomic receptors to castration and testosterone in the urinary bladder of the rabbit

J. Urol.

Pharmacology of lower urinary tract smooth muscles and penile erectile tissues

Pharmacol. Rev.

Physiology of penile erection

Physiol. Rev.

Castration enhances NANC nerve-mediated relaxation in rabbit isolated corpus cavernosum

Acta Physiol. Scand.

Colonic motor and vascular responses to pelvic nerve stimulation and their relation to local peptide release in the cat

J. Physiol.

Gonadal steroid induction of structural sex differences in the central nervous system

Annu. Rev. Neurosci.

Vesicular acetylcholine transporter (VAChT) protein: A novel and unique marker for cholinergic neurons in the central and peripheral nervous systems

J. Comp. Neurol.

The extrinsic innervation of the abdominal organs of the female rat

Acta Anat.

The extrinsic innervation of the pelvic organs in the female rat

Anat. Rec.

Structure of autonomic ganglia

Recovery of choline acetyltransferase activity in the rat urinary bladder deprived of half of its innervation

Acta Physiol. Scand.

Afferent and sympathetic neurons projecting into the lumbar visceral nerves of the male rat

J. Comp. Neurol.

The afferent and sympathetic components of the lumbar spinal outflow to the colon and pelvic organs in the cat. III. The colonic nerves, incorporating an analysis of all components of the lumbar prevertebral outflow

J. Comp. Neurol.

The afferent and sympathetic components of the lumbar spinal outflow to the colon and pelvic organs in the cat. I. The hypogastric nerve

J. Comp. Neurol.

Paraganglienzellen in Ganglion cervicale uteri der Maus

Z. Zeitschrift.

Observations on the loss of catecholamine fluorescence from intrauterine adrenergic nerves during pregnancy in the guinea-pig

J. Reprod. Fertil.

Localisation of norepinephrine and acetylcholinesterase in separate neurons supplying the guinea-pig vas deferens

J. Pharmacol. Exp. Ther.

Identification of delayed potassium and calcium current in the rat sympathetic neuron under voltage-clamp conditions

J. Physiol.

Simultaneous labeling of vagal innervation of the gut and afferent projections from the visceral forebrain with DiI injected into the dorsal vagal complex in the rat

J. Comp. Neurol.

Topography of efferent vagal innervation of the rat gastrointestinal tract

Am. J. Physiol.

Transmission from preganglionic fibres in the hypogastric nerve to peripheral ganglia of male guinea-pigs

J. Physiol.

Three electrophysiological classes of guinea pig sympathetic neurone have distinct morphologies

J. Comp. Neurol.

Electrical and mechanical responses of guinea-pig bladder muscle to nerve stimulation

Br. J. Pharmacol.

Postnatal development of noradrenaline-containing nerves of the rat uterus

J. Auton. Nervous System

Sexual dimorphism in the vertebrate nervous system

J. Neurosci.

Consequence of neonatal androgenization and castration for future levels of norepinephrine transmitter in uterus and vas deferens of the rat

Neuroendocrinology

The purinergic nerve hypothesis

Ciba Foundation Symp.