Both synaptic and antidromic stimulation of neurons in the rat superior cervical ganglion acutely increase tyrosine hydroxylase activity

Abstract

Electrical stimulation of the preganglionic cervical sympathetic trunk produces an acute increase in the rate of DOPA synthesis in the rat superior cervical ganglion. The present study was designed to test the possibility that this acute transsynaptic stimulation of catechol biosynthesis could be, at least in part, a consequence of an increase in the firing rate of the postganglionic sympathetic neurons. For this purpose, the effect of stimulation in vitro of the preganglionic cervical sympathetic trunk was compared to that of stimulation of the predominantly postganglionic internal and external carotid nerves. Stimulation of the cervical sympathetic trunk at 10 Hz for 30 min produced a 4.6-fold increase in DOPA synthesis, while simultaneous stimulation of the two postganglionic trunks produced a 3.1-fold increase. The internal carotid nerve is known to contain a small population of preganglionic fibers that synapse on principal neurons in the ganglion before entering this nerve trunk. To eliminate the possibility that the effect of stimulation of the internal carotid nerve is mediated by synaptic stimulation via these preganglionic ȁthrough fibersȁ, the effect of stimulation of previously decentralized ganglia was examined. While decentralization reduced the magnitude of the effect of stimulation of the internal and external carotid nerves, a 2.0-fold increase in DOPA synthesis was still seen. In addition, when these nerve trunks were stimulated in control ganglia that had been maintained in organ culture for 48 h to allow time for the degeneration of afferent nerve terminals, DOPA synthesis increased 4.1-fold.The increases in DOPA synthesis in ganglia in situ produced by both orthodromic and antidromic stimulation were accompanied by increases in the activation of the enzyme tyrosine hydroxylase measured in ganglion homogcnates. In addition, increases in norepinephrine and dopamine levels were seen. As a first step in an examination of the possibility that the increase in catechol synthesis produced by antidromic stimulation results from an influx of Ca2+ ions, decentralized ganglia and ganglia maintained in organ culture were stimulated antidromically in a low Ca2+/high Mg2+ medium. This change in the ionic composition of the medium completely abolished the effects of antidromic stimulation in decentralized ganglia and reduced the effect of antidromic stimulation of organ-cultured ganglia by about 90%.These data indicate that an increase in the firing rate of sympathetic neurons per se, in the absence of synaptic stimulation, can lead to an increase in tyrosine hydroxylase activity, and they raise the possibility that this biochemical change is mediated by an influx of Ca2+ ions.