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Wilfrid Jänig - One of the best experts on this subject based on the ideXlab platform.
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Non-nicotinic transmission in Autonomic Ganglia revisited – an important physiological function?
The Journal of Physiology, 2005Co-Authors: Wilfrid JänigAbstract:Autonomic Ganglia, in particular sympathetic ones, have fascinated investigators since ancient times. It was believed that these structures are ‘little brains’ that integrate, carry and distribute the ‘animal spirits’ from the brain to the periphery leading to coordinated actions of the peripheral target organs (the ‘sympathies’) in association with the activity of the brain (McLachlan, 1995). However, their primary function is to distribute messages to the periphery from relatively small pools of preganglionic neurones to large pools of postganglionic neurones. Integration occurs in some sympathetic pathways of prevertebral Ganglia (Janig, 1995). The primary transmitter in all Ganglia is acetylcholine (ACh) acting on nicotinic receptors. ACh released by preganglionic fibres also acts on muscarinic receptors and preganglionic fibres may release neuropeptides, both generating slow excitatory synaptic potentials (EPSPs) in some types of postganglionic neurone by decrease of potassium conductance (M currents). What is the function of these slow EPSPs in postganglionic neurones? The paper by Morris et al. (2005) in this issue of The Journal of Physiology describes experiments on an in vitro preparation of the anterior pelvic (paracervical) Ganglia with attached uterine artery and nerves that contain the preganglionic sympathetic or parasympathetic axons innervating the postganglionic vasodilator (VD) neurones to the uterine artery. Repetitive electrical stimulation of the preganglionic axons dilates the artery. This preganglionically induced VD is generated by release of NO and VIP, outlasts the train of stimuli by more then 10 min, and is only slightly reduced in amplitude and delayed after complete block of nicotinic transmission in the paracervical Ganglia. It is generated by continuous discharge of the postganglionic VD neurones produced by a slow EPSP. The transmitter involved is unknown (but unlikely to be substance P, ATP, 5-HT, glutamate or ACh (muscarinic action)). The continuous discharge of the postganglionic neurones cannot be due to a long-term potentiation of cholinergic nicotinic transmission since VD neurones in the paracervical Ganglia receive synaptic inputs from two preganglionic fibres, one being strong (i.e. always suprathreshold). The results of Morris et al. (2005) compare with those obtained more than 20 years ago in vivo in the cat. Repetitive electrical stimulation of preganglionic axons in the lumbar sympathetic trunk (LST; 50 stimuli at 25 Hz) elicits, in a decentralized preparation, early high frequency discharges and late cholinergic mucarinic and/or non-cholinergic long-lasting afterdischarges in many postganglionic neurones supplying the cat hindlimb (Fig. 1B). These afterdischarges can only be elicited when small-diameter (largely unmyelinated) preganglionic axons are stimulated (Janig et al. 1984); they require trains of 50 stimuli of at least 3–4 Hz or 3–10 stimuli at 25 Hz, and only occur in vasoconstrictor (VC) neurones (most muscle (MVC) and some 30% cutaneous VC neurones) but not in sudomotor or pilomotor neurones (Hoffmeister et al. 1978). In a preparation with intact LST the rate of ongoing activity in VC neurones is enhanced for 4–40 min or longer following repetitive stimulation of the small-diameter preganglionic axons (Fig. 1C). This enhancement can also be elicited heterosynaptically and is associated with a long-lasting decrease of blood flow (Blumberg & Janig, 1983; Janig & Koltzenburg, 1991). Stimulation of arterial chemoreceptors by hypoxia (8% O2 in N2) excites MVC neurones. This reflex excitation is also present in many MVC neurones after blockade of nicotinic transmission or of both nicotinic and muscarinic transmission (Fig. 1D) (Janig et al. 1983). Figure 1 Muscarinic and non-cholinergic responses elicited in postganglionic vasoconstrictor neurones (skin (CVC), muscle (MVC)) projecting to the cat hindlimb by activation of preganglionic neurones In conclusion, non-nicotinic (muscarinic and/or peptidergic) synaptic transmission in postganglionic VC neurones may be important under certain functional conditions (Fig. 1E). Infrequent bursts of impulses in preganglionic neurones with slowly conducting axons that converge on postganglionic VC neurones are necessary to generate a long-term increase in ongoing activity in postganglionic VC neurones. This may also apply to the VD and secretomotor pathways supplying the internal reproductive organs in females, leading via a non-cholinergic mechanism in paracervical Ganglia to long-lasting effector responses (vasodilatation, secretion) as shown by Morris et al. (2005). These results tie up with observations in the cat that preganglionic non-VC neurones projecting in lumbar splanchnic nerves can be activated reflexly for 1–12 min after mechanical stimulation of sacral afferents for 20 s (e.g. from the anal canal; Bahr et al. 1986). The mechanism underlying this unique reflex activation that outlasts the afferent stimulus by many minutes is most likely to lie within the spinal pathways. Thus, it may be hypothesized that a centrally potentiated reflex in preganglionic neurones, that probably have VD and secretomotor function, is further amplified by non-cholinergic synaptic transmission in paracervical Ganglia. This sequential cascade of amplification of a central signal might turn out to be of considerable importance in the regulation of the reproductive organs.
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non nicotinic transmission in Autonomic Ganglia revisited an important physiological function
The Journal of Physiology, 2005Co-Authors: Wilfrid JänigAbstract:Autonomic Ganglia, in particular sympathetic ones, have fascinated investigators since ancient times. It was believed that these structures are ‘little brains’ that integrate, carry and distribute the ‘animal spirits’ from the brain to the periphery leading to coordinated actions of the peripheral target organs (the ‘sympathies’) in association with the activity of the brain (McLachlan, 1995). However, their primary function is to distribute messages to the periphery from relatively small pools of preganglionic neurones to large pools of postganglionic neurones. Integration occurs in some sympathetic pathways of prevertebral Ganglia (Janig, 1995). The primary transmitter in all Ganglia is acetylcholine (ACh) acting on nicotinic receptors. ACh released by preganglionic fibres also acts on muscarinic receptors and preganglionic fibres may release neuropeptides, both generating slow excitatory synaptic potentials (EPSPs) in some types of postganglionic neurone by decrease of potassium conductance (M currents). What is the function of these slow EPSPs in postganglionic neurones? The paper by Morris et al. (2005) in this issue of The Journal of Physiology describes experiments on an in vitro preparation of the anterior pelvic (paracervical) Ganglia with attached uterine artery and nerves that contain the preganglionic sympathetic or parasympathetic axons innervating the postganglionic vasodilator (VD) neurones to the uterine artery. Repetitive electrical stimulation of the preganglionic axons dilates the artery. This preganglionically induced VD is generated by release of NO and VIP, outlasts the train of stimuli by more then 10 min, and is only slightly reduced in amplitude and delayed after complete block of nicotinic transmission in the paracervical Ganglia. It is generated by continuous discharge of the postganglionic VD neurones produced by a slow EPSP. The transmitter involved is unknown (but unlikely to be substance P, ATP, 5-HT, glutamate or ACh (muscarinic action)). The continuous discharge of the postganglionic neurones cannot be due to a long-term potentiation of cholinergic nicotinic transmission since VD neurones in the paracervical Ganglia receive synaptic inputs from two preganglionic fibres, one being strong (i.e. always suprathreshold). The results of Morris et al. (2005) compare with those obtained more than 20 years ago in vivo in the cat. Repetitive electrical stimulation of preganglionic axons in the lumbar sympathetic trunk (LST; 50 stimuli at 25 Hz) elicits, in a decentralized preparation, early high frequency discharges and late cholinergic mucarinic and/or non-cholinergic long-lasting afterdischarges in many postganglionic neurones supplying the cat hindlimb (Fig. 1B). These afterdischarges can only be elicited when small-diameter (largely unmyelinated) preganglionic axons are stimulated (Janig et al. 1984); they require trains of 50 stimuli of at least 3–4 Hz or 3–10 stimuli at 25 Hz, and only occur in vasoconstrictor (VC) neurones (most muscle (MVC) and some 30% cutaneous VC neurones) but not in sudomotor or pilomotor neurones (Hoffmeister et al. 1978). In a preparation with intact LST the rate of ongoing activity in VC neurones is enhanced for 4–40 min or longer following repetitive stimulation of the small-diameter preganglionic axons (Fig. 1C). This enhancement can also be elicited heterosynaptically and is associated with a long-lasting decrease of blood flow (Blumberg & Janig, 1983; Janig & Koltzenburg, 1991). Stimulation of arterial chemoreceptors by hypoxia (8% O2 in N2) excites MVC neurones. This reflex excitation is also present in many MVC neurones after blockade of nicotinic transmission or of both nicotinic and muscarinic transmission (Fig. 1D) (Janig et al. 1983). Figure 1 Muscarinic and non-cholinergic responses elicited in postganglionic vasoconstrictor neurones (skin (CVC), muscle (MVC)) projecting to the cat hindlimb by activation of preganglionic neurones In conclusion, non-nicotinic (muscarinic and/or peptidergic) synaptic transmission in postganglionic VC neurones may be important under certain functional conditions (Fig. 1E). Infrequent bursts of impulses in preganglionic neurones with slowly conducting axons that converge on postganglionic VC neurones are necessary to generate a long-term increase in ongoing activity in postganglionic VC neurones. This may also apply to the VD and secretomotor pathways supplying the internal reproductive organs in females, leading via a non-cholinergic mechanism in paracervical Ganglia to long-lasting effector responses (vasodilatation, secretion) as shown by Morris et al. (2005). These results tie up with observations in the cat that preganglionic non-VC neurones projecting in lumbar splanchnic nerves can be activated reflexly for 1–12 min after mechanical stimulation of sacral afferents for 20 s (e.g. from the anal canal; Bahr et al. 1986). The mechanism underlying this unique reflex activation that outlasts the afferent stimulus by many minutes is most likely to lie within the spinal pathways. Thus, it may be hypothesized that a centrally potentiated reflex in preganglionic neurones, that probably have VD and secretomotor function, is further amplified by non-cholinergic synaptic transmission in paracervical Ganglia. This sequential cascade of amplification of a central signal might turn out to be of considerable importance in the regulation of the reproductive organs.
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The Integrative Action of the Autonomic Nervous System: Impulse transmission through Autonomic Ganglia
Integrative Action of the Autonomic Nervous System, 1Co-Authors: Wilfrid JänigAbstract:Postganglionic neurons are the final Autonomic motoneurons. Their cell bodies are aggregated in peripheral Autonomic Ganglia. They receive synaptic input from preganglionic neurons and in some Ganglia (notably sympathetic prevertebral Ganglia) from peripheral neurons of the enteric nervous system and from peptidergic spinal afferent fibers. As already mentioned in Chapter 1, most sympathetic Ganglia are located at distance from their target cells and parasympathetic Ganglia are located close to their targets. Sympathetic Ganglia have fascinated investigators since ancient times. It was believed that these structures are “little brains,” which integrate, carry and distribute the “animal spirits” from the brain to the periphery, leading to coordinated actions of the peripheral target organs (the “sympathies”) in association with the activity of the brain (Fulton 1949; Pick 1970; Spillane 1981; Karczmar et al . 1986). However, it turns out that the primary function of most peripheral sympathetic and parasympathetic pathways is to distribute messages to the periphery from relatively small pools of preganglionic neurons to relatively large pools of postganglionic neurons. This particularly applies to the neural regulation of Autonomic body functions, which are chiefly under central control, e.g., regulation of systemic blood pressure, thermoregulation, gastrointestinal functions, evacuative functions (micturition, defecation), erection, salivation, pupil diameter etc. Acetylcholine is released by all preganglionic axon terminals at their synapses in Ganglia and the effects of nerve activity are antagonized by blockade of nicotinic acetylcholine receptors.
V. I. Skok - One of the best experts on this subject based on the ideXlab platform.
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Nicotinic acetylcholine receptors in Autonomic Ganglia.
Autonomic neuroscience : basic & clinical, 2002Co-Authors: V. I. SkokAbstract:Although alpha3beta4 subunit combination is clearly prevalent in the nAChRs of Autonomic Ganglia neurons, the Ganglia are strikingly different in the ratio of neurons containing each particular nAChR subunit, as found with immunohistochemical methods and from the analysis of the effects of nAChR subunit-specific antibodies on the ACh-induced membrane currents. In particular, the number of neurons containing alpha3, alpha4, alpha5 or alpha7 subunits is by about three times higher in sympathetic Ganglia than in parasympathetic Ganglia. This difference may explain why the parasympathetic and sympathetic Ganglia markedly differ in their pharmacology. Still, alpha7 subunit makes the highest contribution to ACh-induced membrane current. No correlation between the physiological functions of the Ganglia and subunit composition of their nAChRs has been found as yet. High permeability for Ca2+ should permit the nAChRs with alpha7 subunits to influence a variety of Ca2+-dependent events in Autonomic neurons. As found with biochemical methods and site-directed mutagenesis, the ACh binding site is formed in the alpha/beta subunits interface by multiple loops containing cysteine, tyrosine and tryptophan amino residues as important for ACh binding. Likewise, both alpha and beta subunits are important for the effects of blocking agents on nAChRs. As found by electrophysiological methods, each neuron of sympathetic and parasympathetic Ganglia, as a rule, possesses nAChRs of two groups, "fast" and "slow", with the mean duration of the burst of single channel openings ranging approximately from 5 to 10 and from 25 to 45 ms, respectively. These groups of channels differ from each other with their pharmacology. The burst-like activity of Autonomic nAChRs channels is possible only if the disulfide bonds are left intact, otherwise only single openings of the channel are observed. The ionic channel of a nAChRs pentamer is formed by M2 transmembrane segments arranging glutamate, serine, threonine, leucine, and valine rings critical for channel conductance and ionic selectivity. In particular, the mutations V251T and E237A, and insertion of proline or alanine, convert a cation-selective channel into an anion-selective one. The open-channel blockers bind to the nAChR channel at the level where the channel diameter is nearly 12 A, both for "fast" and "slow" channel groups.
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Subunit Composition of Nicotinic Acetylcholine Receptors in the Neurons of Autonomic Ganglia
Neurophysiology, 2002Co-Authors: V. I. SkokAbstract:The distribution of α subunits in different parts of the Autonomic nervous system and the correlation between physiological functions of Autonomic ganglion neurons and subunit composition of the nAChR are the subjects of their analysis. In particular, it was found that functionally different Autonomic Ganglia differ from each other in the α subunit composition of their nAChR, and the sensitivity of the nAChR to specific antibodies is markedly variable even within the same ganglion.
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Alpha subunit composition of nicotinic acetylcholine receptors in the rat Autonomic Ganglia neurons as determined with subunit-specific anti-α(181–192) peptide antibodies
Neuroscience, 1999Co-Authors: Maryna Skok, L. P. Voitenko, S. V. Voitenko, E. Y. Lykhmus, E.n. Kalashnik, T.i. Litvin, S.j. Tzartos, V. I. SkokAbstract:Abstract The subunit composition of nicotinic acetylcholine receptors of rat Autonomic Ganglia neurons was studied by means of antibodies, which differentiated between different α subunits and specifically blocked acetylcholine-induced membrane currents. Polyclonal rabbit antibodies and mouse monoclonal antibodies were raised against synthetic peptides matching in sequence the α(181–192) region of α3, α4, α5, and α7 subunits of rat neuronal nicotinic acetylcholine receptors. The antibodies discriminated among α3, α4, α5, and α7 peptides in enzyme-linked immunosorbent assay and bound to native acetylcholine receptors expressed in PC-12 cells. By means of immunoperoxidase staining of cultured rat Autonomic neurons followed by transmission, dark-field and phase-contrast microscopy, it was found that all cells of the superior cervical Ganglia expressed the α3, α5, and α7 nicotinic acetylcholine receptors, whereas approximately half of the cells were clearly α4-positive. In contrast, only about one-third of the intracardiac neurons were α3-positive, about 50% were α4-positive, one-seventh were α5-positive, and one-fifth were α7-positive. All antibodies tested blocked acetylcholine-induced currents in the neurons of the superior cervical Ganglia as was demonstrated by whole-cell patch-clamp studies. Although each antibody could block up to 80% of the current, the degree of inhibition varied considerably from cell to cell. It is concluded that α3, α5, and α7 subunits are expressed in all neurons of the superior cervical ganglion and in some intracardiac neurons, whereas α4 subunits are expressed in some but not all neurons of both tissues. The neurons of the superior cervical ganglion express heterogeneous acetylcholine receptors and differ in relative amounts of acetylcholine receptor subtypes expressed.
Steven L Carroll - One of the best experts on this subject based on the ideXlab platform.
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neurotrophin sensitivity of prevertebral and paravertebral rat sympathetic Autonomic Ganglia
Journal of Neuropathology and Experimental Neurology, 1998Co-Authors: Lee A Selznick, Steven L Carroll, Peter S Distefano, Robert E Schmidt, Denise A DorseyAbstract:Prevertebral and paravertebral sympathetic Autonomic Ganglia respond differently to a large number of experimental and clinical insults. The selective involvement of subpopulations of sympathetic neurons may reflect differences in their response to neurotrophic substances. To test this hypothesis, we investigated the response of prevertebral and paravertebral rat sympathetic Ganglia to selected neurotrophic substances in vivo and in vitro and identified the ganglionic distribution of neurons expressing high affinity neurotrophin receptor mRNAs. Dissociated cultures of embryonic prevertebral and paravertebral ganglionic neurons showed comparable responses to NGF deprivation and only small differences in their response to rescue with other trophic substances. In situ hybridization studies of adult rat sympathetic Ganglia using probes specific for the high-affinity neurotrophin receptor transcripts trks A, B, and C demonstrated that neurons in both prevertebral and paravertebral sympathetic Ganglia express predominantly trkA receptors in vivo. In addition, increased tyrosine hydroxylase (TOH) activity was induced only by doses of neurotrophic substances that activate trkA and showed only small differences between neonatal prevertebral and paravertebral Ganglia. Although small differences in the sensitivity of pre- and paravertebral sympathetic neurons to various neurotrophins have been identified in our studies, they are unlikely, in isolation, to explain major differences in the sensitivity of these Ganglia to neuropathologic processes.
Robert E Schmidt - One of the best experts on this subject based on the ideXlab platform.
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neurotrophin sensitivity of prevertebral and paravertebral rat sympathetic Autonomic Ganglia
Journal of Neuropathology and Experimental Neurology, 1998Co-Authors: Lee A Selznick, Steven L Carroll, Peter S Distefano, Robert E Schmidt, Denise A DorseyAbstract:Prevertebral and paravertebral sympathetic Autonomic Ganglia respond differently to a large number of experimental and clinical insults. The selective involvement of subpopulations of sympathetic neurons may reflect differences in their response to neurotrophic substances. To test this hypothesis, we investigated the response of prevertebral and paravertebral rat sympathetic Ganglia to selected neurotrophic substances in vivo and in vitro and identified the ganglionic distribution of neurons expressing high affinity neurotrophin receptor mRNAs. Dissociated cultures of embryonic prevertebral and paravertebral ganglionic neurons showed comparable responses to NGF deprivation and only small differences in their response to rescue with other trophic substances. In situ hybridization studies of adult rat sympathetic Ganglia using probes specific for the high-affinity neurotrophin receptor transcripts trks A, B, and C demonstrated that neurons in both prevertebral and paravertebral sympathetic Ganglia express predominantly trkA receptors in vivo. In addition, increased tyrosine hydroxylase (TOH) activity was induced only by doses of neurotrophic substances that activate trkA and showed only small differences between neonatal prevertebral and paravertebral Ganglia. Although small differences in the sensitivity of pre- and paravertebral sympathetic neurons to various neurotrophins have been identified in our studies, they are unlikely, in isolation, to explain major differences in the sensitivity of these Ganglia to neuropathologic processes.
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Neuropathology of human sympathetic Autonomic Ganglia.
Microscopy research and technique, 1996Co-Authors: Robert E SchmidtAbstract:The neuropathologic alterations which underlie Autonomic nervous system dysfunction in aging and in a variety of diseases have been systematically examined in the sympathetic Ganglia of a series of 347 autopsied adults and in a review of previously published studies. Markedly swollen terminal axons containing neurofilamentous aggregates were found immediately adjacent to the neuronal cell bodies of prevertebral sympathetic Ganglia in aging, in diabetes, and, to a lesser extent, in alcoholism. Dystrophic axons appeared to involve subpopulations of intraganglionic nerve fibers, chiefly those containing neuropeptide Y (NPY), and were more frequent in males than females. Neither aging nor diabetes resulted in significant numbers of actively degenerating neurons or a substantial decrease in neuronal density. Parenchymal aggregates of lymphocytes in the ganglionic neuropil and perivascular regions represented a frequent histologic finding in both prevertebral and paravertebral Ganglia; however, they were not selectively increased in frequency or intensity in diabetic subjects or in any other disease entity. Many dilated clear “vacuoles,” apparently located within the neuronal cell bodies of paravertebral and prevertebral Ganglia according to light microscopy, were subsequently shown by electron microscopy to represent vacuolated or fluid-filled neurites, most likely terminal axons or synapses. Vacuolated neurites were more frequent in, although not confined to, diabetic patients. Similar pathologic findings have been reported in studies of sympathetic Ganglia in various human diseases. The frequency of some pathologic lesions in control populations as a function of age or gender necessitates the careful selection of a relatively large, appropriately matched, control population for comparison with presumed disease-induced ganglionic neuropathology, and emphasizes the importance of quantitative comparisons. © 1996 Wiley-Liss, Inc.
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Fine structure of presynaptic axonal terminals in sympathetic Autonomic Ganglia of aging and diabetic human subjects.
Synapse (New York N.Y.), 1992Co-Authors: Jo Anna Schroer, Santiago B. Plurad, Robert E SchmidtAbstract:The neuropathologic changes that may underlie Autonomic nervous system dysfunction in nondiabetic elderly human subjects or as a complication of diabetes have been systematically examined in sympathetic Ganglia of a series of autopsied human subjects. As in animal models of aging and diabetes, enormously swollen terminal axons were found closely apposed to the perikarya of principal sympathetic neurons in prevertebral superior mesenteric sympathetic Ganglia of aged and diabetic human subjects. Dystrophic axons consisted of two stereotyped forms: the first was composed of large numbers of misalligned aggregates of neurofilaments surrounded by variable numbers of small dense core vesicles; the second was characterized by large numbers of mitochondria, vacuoles, and dense and multivesicular bodies. The fine structural characteristics of neuroaxonal dystrophy, its predilection for prevertebral rather than paravertebral sympathetic Ganglia, and the tendency for multiple dystrophic axons to cluster preferentially around selected neurons were identical in aged and diabetic human Ganglia and were similar to changes seen in animal models of aging and diabetes. Neither diabetic nor aging Ganglia demonstrated evidence of neuronal degeneration. Such structural changes may represent a degenerative influence of diabetes and aging on the normal remodeling of nerve terminals in Autonomic Ganglia, i. e., the continually ongoing process of turnover and replacement of axonal terminals. Similarity of lesions in human diabetes and aging suggests the possibility of pathogenetic mechanisms that are common to diabetes and the aging process. The substantial parallels between humans and animal models provide support for the validity of testing some proposed pathogenetic mechanisms directly in animal models. © 1992 Wiley-Liss, Inc.
Abdulaziz M. Aleisa - One of the best experts on this subject based on the ideXlab platform.
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Plasticity of synaptic transmission in Autonomic Ganglia.
Progress in neurobiology, 2005Co-Authors: Karim A. Alkadhi, Karem H. Alzoubi, Abdulaziz M. AleisaAbstract:Synaptic plasticity is a term that describes long-lasting changes in the efficacy of synaptic transmission resulting from certain patterned activities of the presynaptic nerve. One form of synaptic plasticity, long-term potentiation (LTP), is an activity-dependent marked increase in synaptic efficacy that has been extensively studied in various regions of the central nervous system, particularly the hippocampus, where LTP is widely believed to be a cellular correlate of learning and memory. A similar phenomenon has been identified in sympathetic Ganglia even before Bliss and Lomo coined the term LTP in 1973. Ganglionic LTP (gLTP) of the nicotinic pathway is a similarly long-lasting increase in synaptic effectiveness that can be induced in Ganglia following a brief train of relatively high frequency stimulation (HFS) of the preganglionic nerve. Remarkably similar to the LTP of the hippocampus, gLTP has been demonstrated in Autonomic Ganglia from a number of vertebrates including mammalian, amphibian and avian species. Several other forms of long-lasting increases in synaptic effectiveness have been demonstrated in sympathetic Ganglia following exposure to adrenergic agonists, neuroactive peptides and cyclic nucleotides and even after a challenge by an antigen. The main emphasis of this review, however, will be on the activity-dependent gLTP of the mammalian sympathetic Ganglia, in particular the superior cervical ganglion of the rat. Since the last, excellent and comprehensive review of this ganglionic function by Briggs in 1995, important discoveries about the mechanisms of induction and maintenance of gLTP have been reported, including the finding that the response is uniquely dependent on serotonin for both the induction phase and maintenance phase. These new advances will be discussed in depth in this review.
