Ultrastructural analysis of the distribution of synaptic boutons from labeled preganglionic axons on rabbit ciliary neurons

Forehand, CJ

doi:10.1523/jneurosci.07-10-03274.1987

Cited by 17 publications

(11 citation statements)

References 22 publications

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“…In neurons with a simple morphology, such as amphibian sympathetic and parasympathetic neurons that lack dendrites, a pericellular basket of boutons clearly represents the preganglionic inputs to that cell (McMahan and Kuffler, 1971;Taxi, 1976;Sargent, 1983;Streichert and Sargent, 1989). A similar arrangement occurs in simple mammalian neurons, such as those in the ciliary ganglia of rabbits (Forehand and Purves, 1984;Forehand, 1987). By analogy with these observations, it has been assumed that pericellular baskets in mammalian sympathetic ganglia, usually labelled for immunoreactivity to particular neuropeptides, also represent preganglionic inputs to the neurons they surround (e.g., Heym et al, 1984Heym et al, , 1990Lindh et al, 1986;Yamamoto et al, 1989;Gibbins, 1992;Gibbins and Matthew, 1996).…”

Section: Discussionmentioning

confidence: 93%

Synaptic organisation of neuropeptide-containing preganglionic boutons in lumbar sympathetic ganglia of guinea pigs

et al. 1998

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Within the lumbar sympathetic ganglia of guinea pigs, the endings of different populations of neuropeptide-containing preganglionic neurons form well-defined pericellular baskets of boutons around target neurons in specific functional pathways. We have used multiple-labelling immunofluorescence, confocal microscopy, and ultrastructural immunocytochemistry to investigate synaptic organisation within pericellular baskets labelled for immunoreactivity to calcitonin gene-related peptide (CGRP), substance P (SP), or the pro-enkephalin-derived peptide, met-enkephalin-arg-gly-leu (MERGL) in relation to their target neurons. Different functional populations of neurons, identified by their neurochemical profile, showed a significant degree of spatial clustering and predicted well the distribution of specific classes of pericellular baskets. Most of the boutons in a basket were completely surrounded by Schwann cell processes and did not form synapses. The synapses that were present were made mostly onto dendrites enclosed by the Schwann cell sheath surrounding the neuron within the basket. These dendrites probably originated from neurochemically similar neighbouring neurons. Nevertheless, some of the boutons in the baskets did form synapses with the cell body or proximal dendrites of the neuron they surrounded. Occasionally, cell bodies received a relatively high number of synapses and close appositions from boutons in a pericellular basket. Synaptic convergence of two immunohistochemically distinct types of preganglionic inputs was found in baskets of SP-immunoreactive or MERGL-immunoreactive, but not CGRP-immunoreactive, boutons. Taken together, our results show that the appearance of pericellular baskets is primarily due to the packing of the target neurons. The grouping of functionally similar classes of neurons with their pathway-specific projections of peptide-containing preganglionic neurons suggests that peptides could exert their effects in relatively well-defined zones within the ganglia.

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Section: Discussionmentioning

confidence: 93%

Synaptic organisation of neuropeptide-containing preganglionic boutons in lumbar sympathetic ganglia of guinea pigs

et al. 1998

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“…This result is consistent with the total number of synaptic contacts being proportional to the total surface area of the target neuron. They have further concluded that each dendrite provides a separate domain that, to a large degree, provides an exclusive synaptic target for each preganglionic input (Hume and Purves 1983;Forehand 1987). However, these earlier studies predate the recognition that different populations of preganglionic and intestinofugal inputs to sympathetic neurons can be distinguished by their patterns of neuropeptide expression.…”

Section: "Dendritic Domain" Hypothesismentioning

confidence: 99%

Structure of peripheral synapses: autonomic ganglia

Gibbins

Morris

2006

Cell Tissue Res

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Final motor neurons in sympathetic and parasympathetic ganglia receive synaptic inputs from preganglionic neurons. Quantitative ultrastructural analyses have shown that the spatial distribution of these synapses is mostly sparse and random. Typically, only about 1%-2% of the neuronal surface is covered with synapses, with the rest of the neuronal surface being closely enclosed by Schwann cell processes. The number of synaptic inputs is correlated with the dendritic complexity of the target neuron, and the total number of synaptic contacts is related to the surface area of the post-synaptic neuron. Overall, most neurons receive fewer than 150 synaptic contacts, with individual preganglionic inputs providing between 10 and 50 synaptic contacts. This variation is probably one determinant of synaptic strength in autonomic ganglia. Many neurons in prevertebral sympathetic ganglia receive additional convergent synaptic inputs from intestinofugal neurons located in the enteric plexuses. The neurons support these additional inputs via larger dendritic arborisations together with a higher overall synaptic density. There is considerable neurochemical heterogeneity in presynaptic boutons. Some synapses apparently lack most of the proteins normally required for fast transmitter release and probably do not take part in conventional ganglionic transmission. Furthermore, most preganglionic boutons in the ganglionic neuropil do not form direct synaptic contacts with any neurons. Nevertheless, these boutons may well contribute to slow transmission processes that need not require conventional synaptic structures.

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“…Consequently, the number of convergent synaptic inputs received by a neuron tends to be closely related to the number of dendrites it has. However, these dendritic domains are not absolute, and separate preganglionic fibers may converge onto single dendrites of autonomic final motor neurons (Forehand, 1987;Murphy et al, 1998). In the medial CG, most dendrites receive abundant convergent synapses from preganglionic and intestinofugal inputs.…”

Section: Do Dendrites Form Segregated Domains For Synapse Formation?mentioning

confidence: 99%

“…Most of the final neurons in sympathetic or parasympathetic motor pathways have relatively simple dendritic trees and receive only a small number of convergent synaptic inputs from preganglionic neurons located in the brainstem or spinal cord (Gibbins, 1995;Jä nig, 1995). On average, the number of inputs received by an autonomic final motor neuron is positively correlated with its number of primary dendrites (Purves and Hume, 1981;Hume and Purves, 1983;Forehand, 1987). The overall synaptic density is low, so that around only 1-2% of the surface of the soma and dendrites is covered with synapses.…”

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confidence: 99%

Synaptic density, convergence, and dendritic complexity of prevertebral sympathetic neurons

Gibbins

Teo

Jobling

et al. 2002

J of Comparative Neurology

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Prevertebral sympathetic ganglia contain a unique population of final motor neurons receiving convergent synaptic inputs not only from spinal preganglionic neurons, but also from peripheral intestinofugal neurons projecting from the gut. We used quantitative confocal and ultrastructural immunohistochemistry to determine how this increased synaptic convergence is accommodated by sympathetic final motor neurons in the celiac ganglion of guinea pigs. Terminals of intestinofugal neurons were identified by their immunoreactivity to vasoactive intestinal peptide. Stereologic analyses were based on transects and point counts at confocal and ultrastructural levels. The relative amount of dendritic neuropil in the medial regions of the ganglion was approximately 2.5 times greater than in the lateral regions of the ganglion, consistent with the 2 to 3 times difference in average dendritic field size of neurons in these regions. The total numbers of boutons and synaptic profiles showed significant positive correlations with the relative amount of neuropil in a region. However, the overall density of synaptic boutons was twice as high in the medial region of the ganglion compared with the lateral regions. Because the relative density of preganglionic synapses was similar in each region, this difference was due to the selective projection of intestinofugal inputs to neurons in the medial celiac ganglion, where they provided 45% of synaptic contacts. These results show that, compared with vasoconstrictor neurons, sympathetic neurons regulating gastrointestinal activity support a higher number of convergent inputs in two ways: in addition to having larger dendritic fields, they also have a twofold higher density of synapses.

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Ultrastructural analysis of the distribution of synaptic boutons from labeled preganglionic axons on rabbit ciliary neurons

Cited by 17 publications

References 22 publications

Synaptic organisation of neuropeptide-containing preganglionic boutons in lumbar sympathetic ganglia of guinea pigs

Synaptic organisation of neuropeptide-containing preganglionic boutons in lumbar sympathetic ganglia of guinea pigs

Structure of peripheral synapses: autonomic ganglia

Synaptic density, convergence, and dendritic complexity of prevertebral sympathetic neurons

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