Long‐term potentiation induced by a sustained rise in the intraterminal Ca2+ in bull‐frog sympathetic ganglia.

Abstract

SUMMARY1. The mechanism of a long-term potentiation of transmitter release (pre-LTP) induced by a tetanic stimulation (33 Hz for 1-30 s) applied to the preganglionic nerve was examined by intracellularly recording the fast excitatory postsynaptic potentials (fast EPSPs) in bull-frog sympathetic ganglia.2. Short-term facilitation induced by paired pulses was decreased during the course of pre-LTP; the extent of reduction paralleled with the magnitude of pre-LTP.3. The frequency of miniature EPSPs increased after tetanic stimulation that produced the pre-LTP.4. The Ca2" ionophore, A23187, increased both the amplitude and quantal content of fast EPSPs and frequency of miniature EPSPs while it decreased short-term facilitation.5. A Ca2" chelating agent, Quin-2, loaded as acetoxymethyl ester, reduced the amplitude and quantal content of fast EPSPs and short-term facilitation, and blocked the generation of pre-LTP.6. Activators of protein kinase C, phorbol 12,13-dibutyrate and 1-oleoyl-2-acetylrac-glycerol, and its inhibitors, H-7 and staurosporine, did not block the generation of pre-LTP, while the activators enhanced transmitter release.7. Inhibitors of calmodulin, trifluoperazine and W-7, blocked the generation of pre-LTP, whereas the amplitude and quantal content of fast EPSPs were not influenced.8. These results suggest that the pre-LTP results from a sustained rise in the basal level of intraterminal Ca2' and an activation of the Ca2+-calmodulin-dependent process in the preganglionic nerve terminals.

The effect of ions and second messengers on long‐term potentiation of chemical transmission in avian ciliary ganglia

“…Therefore, the maximum amplitude of LTP and PTP is directly proportional to the frequency of stimulation as this affects the amount of overlap and summation of the inward presynaptic calcium signal. The PTP following the tetanus of 30 Hz for 20 s declined with a time constant of about 1.5 min, which is similar to that at other ganglionic synapses (Waziri et al, 1969;Zengel et al, 1980), as is the time constant of decline of the LTP of about 50 min (Dunant & Dolivo, 1968;Brown & McAfee, 1982;Briggs et al, 1985;Briggs & McAfee, 1988;Minota et al, 1991). During potentiation, elevated calcium levels in the presynaptic nerve terminal (Zucker, 1989;Kuba & Kumamoto, 1990;Swandulla et al, 1991) …”

“…This implies that calcium concentration in the presynaptic nerve terminal is raised for the induction but not the maintenance of LTP in the ciliary ganglion. Short term-facilitation is also reduced during LTP at bullfrog sympathetic preganglionic nerve terminals but this lasts for the entire period of LTP (Minota et al, 1991), and therefore suggests that intraterminal calcium is elevated during LTP here. However at mossy fibre terminals on CA3 pyramidal neurones the intraterminal calcium concentration is only elevated during the first few minutes of LTP (Zalutsky & Nicholl, 1990).…”

“…This LTP is likely to be due to an enhanced probability of secretion of quanta from the nerve terminal as there is no change in the sensitivity of the postsynaptic membrane to applied acetylcholine (Briggs & McAfee, 1988) and an accompanying increase in quantal content (Briggs et al, 1985;Koyano et al, 1985). This LTP is thought to be the result of an elevated calcium concentration in the preganglionic nerve terminals of both amphibia and mammals following a tetanus, as short term facilitation is substantially decreased during LTP (Minota et al, 1991); the amplitude of LTP is also dependent on the level of the extracellular calcium concentration (Briggs et al, 1985).…”

Induction and maintenance of ganglionic long‐term potentiation require activation of 5‐hydroxytryptamine (5‐HT3) receptors.

“…This is in contrast to the frog sympathetic ganglion in which similar experiments indicate elevation of intraterminal Ca2P throughout LTP (Minota, Kumamoto, Kitakoga & Kuba, 1991). The status of intraterminal Ca2P concentration during PTP and LTP in the mammalian sympathetic ganglia remains to be studied.…”

Neurotransmission through sympathetic ganglia of spontaneously hypertensive rats.

“…Specifically, an increase in quantal content has been shown to produce larger excitatory postsynaptic potentials, which due to transmitter depletion display decreased facilitation and greater depression during trains of activity. 28 - 29 Also, the previously reported decreased dopamine concentrations could play a role in the enhanced transmission observed at low frequencies by decreasing the inhibitory influence of dopamine on the postganglionic neurons. However, one would also suspect that this decreased inhibition would also be present at the higher frequencies.…”