Synaptic transmission without action potentials: input-output properties of a nonspiking presynaptic neuron

Abstract

1. Input-output properties of the inhibitory synaptic connection between non-spiking neurons (EX1) and gastric mill (GM) neurons were examined in the stomatogastric ganglion of the spiny lobster, Panulirus interruptus. Current was injected into and the voltage was recorded during current injection, two independent microelectrodes were used. 2. The EX1-GM synaptic connection is a conductance-increase inhibitory type, with an input-output curve that resembles the curve for the squid giant synapse. There is a threshold level of depolarization for transmitter release from the presynaptic cell. Beyond that threshold, increasing presynaptic depolarization causes increasing postsynaptic hyperpolarization (and inhibition). 3. A long presynaptic current step always causes a postsynaptic response with an initial peak of hyperpolarization followed by a decay to a less hyperpolarized plateau level. The plateau level is maintained, in most cells, for the duration of the presynaptic depolarization even over long periods (30 s). 4. The peak, but not the plateau, part of the postsynaptic response is sensitive to the past history of the synaptic connection. If a large conditioning pulse is applied to the presynaptic cell causing a large postsynaptic hyperpolarization, then the postsynaptic response to a later presynaptic test depolarization will have a reduced peak, leaving the plateau component unchanged.

Temporal Dynamics of Graded Synaptic Transmission in the Lobster Stomatogastric Ganglion

“…Almost all of the previously published work studying graded synaptic transmission in the stomatogastric nervous system used single, long, square presynaptic current pulses (Maynard and Walton, 1975;Graubard, 1978;Graubard et al, 1980Graubard et al, , 1983Johnson and Harris-Warrick, 1990;Johnson et al, 1991Johnson et al, , 1995. Our study reveals that the amplitude of the postsynaptic response depends on the specific shape of the presynaptic waveform.…”

“…The threshold for transmitter release is close to the resting potential, and synaptic release is both spike-mediated and graded (Maynard and Walton, 1975;Graubard, 1978;Graubard et al, 1980Graubard et al, , 1983Johnson and Harris-Warrick, 1990;Johnson et al, 1995). At some synapses the graded component of transmitter release is significantly larger than that evoked by action potentials and is the major contributor to network dynamics (Raper, 1979;Graubard et al, 1983;Hartline et al, 1988).…”

“…Graded synaptic transmission between pyloric neurons has been extensively studied in a "static" context in which the time dependence of the transmission was ignored (Graubard, 1978;Graubard et al, 1980Graubard et al, , 1983Johnson and Harris-Warrick, 1990;Johnson et al, 1995). However, graded synaptic transmission between pyloric neurons shows depression and depends on the amplitude, frequency, and shape of the depolarization of the presynaptic neuron (Graubard et al, 1989;Hartline and Graubard, 1992).…”

Synaptic Dynamics Do Not Determine Proper Phase of Activity in a Central Pattern Generator

“…Previous studies have shown the usefulness of single, long, square pulses in the study of graded synaptic transmission in the STNS (Maynard and Selverston, 1975;Graubard, 1978;Johnson and HarrisWarrick, 1990;Manor et al, 1997). Figure 2 A shows simultaneous responses of the LP (middle trace) and PY (bottom trace) neurons to a 2 s presynaptic square pulse in both PD neurons from Ϫ60 to Ϫ20 mV (top trace) in TTX saline.…”

“…The inhibitory synapses between the pacemaker ensemble and the LP and PY neurons use voltage-dependent (graded) release of neurotransmitter as the major form of transmission (Maynard and Walton, 1975;Graubard, 1978;Graubard et al, 1980;Johnson and Harris-Warrick, 1990;Johnson et al, 1995). To isolate this form of synaptic release, spikemediated transmission was blocked by superfusing the preparation with Panulirus saline containing 10 Ϫ7 M TTX (Biotium, Hayward, CA).…”