The synaptic organization of the prepacemaker nucleus in weakly electric knifefish, Eigenmannia: a quantitative ultrastructural study.
Weakly electric knifefish (Eigenmannia sp.) produce continuous electric organ discharges at very constant frequencies. Modulations of the discharges occur during social interactions and are under control of the diencephalic prepacemaker nucleus. Abrupt frequency modulations, or 'chirps', which are observed predominantly during the breeding season, can be elicited by stimulation of neurons in a ventro-lateral portion of the prepacemaker nucleus, the so-called PPn-C. The PPn-C consists of approximately 100 loosely scattered large multipolar neurons which send dendrites into three territories, called 'dorso-medial', 'dorso-lateral', and 'ventral'. In the present ultrastructural investigation, the synaptic organization of these neurons, identified by retrograde labelling with horseradish peroxidase, was studied quantitatively. Somata and dendrites of the PPn-C receive input from two classes of chemical synapses. Class-1 boutons contain predominantly agranular, round vesicles and are believed to be excitatory. Class-2 boutons display predominantly flattened or pleiomorphic vesicles and are probably inhibitory. The action of the agranular vesicles in the synaptic boutons of these two classes may be modulated by the content of large dense-core vesicles. These comprise approximately 1% of the total vesicle population and are found predominantly in regions distant from the active zone of the synaptic bouton. The density of chemical synapses exhibits marked topographic differences. Class-1 boutons occur typically at densities of 3-12 synapses per 100 microns of profile length on dendrites and cell bodies. No significant differences in density of class-1 boutons could be found between distal dendrites of the three territories, proximal dendrites and cell bodies. The density of class-2 synapses, on the other hand, increases significantly from usually less than 1 synapse per 100 microns of profile length on distal dendrites to 2-3 synapses per 100 microns of profile length on proximal dendrites and cell bodies. Such a topographic organization could enable the proximal elements to 'veto' the depolarizing response of distal dendrites to excitatory inputs. The growth of dendrites in the dorso-medial territory during the breeding season, as shown in a previous study, and the concurrent doubling of excitatory input received by class-1 synapses, could overcome the inhibition caused on somata and proximal dendrites by class-2 synapses and thus account for the dramatic increase in the fish's propensity to chirp in the context of sexual maturity.
Zupanc
G K
GK
Department of Neurosciences, School of Medicine, University of California, San Diego, La Jolla 92093-0202.
D000818:Animals; D001921:Brain / Q000648:ultrastructure*; D004027:Diencephalon / Q000648:ultrastructure; D004555:Electric Fish / Q000033:anatomy & histology* / Q000502:physiology; D004557:Electric Organ / Q000502:physiology; D008636:Mesencephalon / Q000648:ultrastructure; D008854:Microscopy, Electron; D009474:Neurons / Q000648:ultrastructure*; D013569:Synapses / Q000648:ultrastructure*; D013572:Synaptic Vesicles / Q000648:ultrastructure