Development of convergent synaptic inputs to subpopulations of autonomic neurons.
Visceromotor neurons in mammalian prevertebral sympathetic ganglia receive convergent synaptic inputs from spinal preganglionic neurons and peripheral intestinofugal neurons projecting from the enteric plexuses. Vasomotor neurons in the same ganglia receive only preganglionic inputs. How this pathway-specific pattern of connectivity is established is unknown. We have used a combination of immunohistochemical, ultrastructural, and electrophysiological techniques to investigate the development of synaptic inputs onto visceromotor and vasomotor neurons in the celiac ganglion of guinea pigs. Functional synaptogenesis occurred primarily from early fetal (F30-F35) to midfetal (F36-F45) stages, after the neurochemical differentiation of vasomotor and visceromotor neurons but before establishment of their electrophysiological phenotypes. Intestinofugal inputs were detected only on presumptive visceromotor neurons located primarily in medial regions of the ganglion. The number of ultrastructurally identified synaptic profiles increased in parallel with functional synaptogenesis, especially in medial regions, where dendritic growth rates also were higher. However, the expression of immunoreactivity to choline acetyltransferase in the terminals of inputs was very low until late fetal stages, after functional transmission already had been established. These results show that peripheral intestinofugal neurons directly establish appropriate functional connections with their target visceromotor neurons simultaneously with the development of functional preganglionic inputs to both visceromotor and vasomotor neurons. It seems likely that synaptogenesis occurs independently of the neurochemical differentiation of the target neurons but is closely related to the pathway-specific dendritic development of those neurons.
Anderson
Rebecca L
RL
Department of Anatomy and Histology and Centre for Neuroscience, Flinders Medical Research Institute, The Flinders University of South Australia, Adelaide, South Australia, 5001 Australia. rebecca.anderson@flinders.edu.au
Jobling
Phillip
P
Matthew
Sue E
SE
Gibbins
Ian L
IL
D000109:Acetylcholine / Q000378:metabolism; D000200:Action Potentials / Q000502:physiology; D000818:Animals; D000831:Animals, Newborn; D002454:Cell Differentiation / Q000502:physiology*; D002795:Choline O-Acetyltransferase / Q000378:metabolism; D003712:Dendrites / Q000502:physiology / Q000648:ultrastructure; D004064:Digestive System / Q000294:innervation; D004068:Digestive System Physiological Phenomena; D017615:Enteric Nervous System / Q000196:embryology* / Q000254:growth & development / Q000648:ultrastructure; D019706:Excitatory Postsynaptic Potentials / Q000502:physiology; D005260:Female; D005333:Fetus; D005728:Ganglia, Sympathetic / Q000196:embryology* / Q000254:growth & development / Q000648:ultrastructure; D020439:Growth Cones / Q000502:physiology / Q000648:ultrastructure; D006168:Guinea Pigs / Q000196:embryology* / Q000254:growth & development / Q000378:metabolism; D009434:Neural Pathways / Q000196:embryology* / Q000254:growth & development / Q000648:ultrastructure; D009478:Neuropeptide Y / Q000378:metabolism; D010641:Phenotype; D011247:Pregnancy; D017729:Presynaptic Terminals / Q000502:physiology / Q000648:ultrastructure*; D013153:Splanchnic Nerves / Q000196:embryology* / Q000254:growth & development / Q000648:ultrastructure; D009435:Synaptic Transmission / Q000502:physiology; D014660:Vasoactive Intestinal Peptide / Q000378:metabolism
D009478:Neuropeptide Y; D014660:Vasoactive Intestinal Peptide; D002795:Choline O-Acetyltransferase; D000109:Acetylcholine