Dopamine activates two different receptors to produce variability in sign at an identified synapse

Chemical synaptic transmission was investigated at a central synapse betwee n identified neurons in the freshwater snail, Lymnaea stagnalis. The presyn aptic neuron was the dopaminergic cell, Right Pedal Dorsal one (RPeD1). The postsynaptic neuron was Visceral Dorsal four (VD4). These neurons ate comp onents of the respiratory central pattern generator. The synapse from RPeD1 to VD4 showed variability of sign, i.e., it was either inhibitory (monopha sic and hyperpolarizing), biphasic (depolarizing followed by hyperpolarizin g phases), or undetectable. Both the inhibitory and biphasic synapse were e liminated by low Ca2+/high Mg2+ saline and maintained in high Ca2+/high Mg2 + saline, indicating that these two types of connections were chemical and monosynaptic. The latency of the inhibitory postsynaptic potential (IPSP) i n high Ca2+/high Mg2+ saline was similar to 43 ms. whereas the biphasic pos tsynaptic potential (BPSP) had similar to 12-ms latency in either normal or high Ca2+/high Mg2+ saline. For a given preparation, when dopamine was pre ssured applied to the soma of VD4, it always elicited the same response as the synaptic input from RPeD1. Thus, for a VD4 neuron receiving an IPSP fro m RPeD1, pressure application of dopamine to the soma of VD4 produced an in hibitory response similar to the IPSP. The reversal potentials of the IPSP and the inhibitory dopamine response were both approximately -90 mV. For a VD4 neuron with a biphasic input from RPeD1, pressure-applied dopamine prod uced a biphasic response similar to the BPSP. The reversal potentials of th e depolarizing phase of the BPSP and the biphasic dopamine response were bo th approximately -44 mV, whereas the reversal potentials for the hyperpolar izing phases were both approximately -90 mV. The hyperpolarizing but not th e depolarizing phase of the BPSP and the biphasic dopamine response was blo cked by the D-2 dopaminergic antagonist(+/-) sulpiride. Previously, our lab oratory demonstrated that both IPSP and the inhibitory dopamine response ar e blocked by (+/-) sulpiride. Conversely, the depolarizing phase of both th e BPSP and the biphasic dopamine response was blocked by the Cl- channel an tagonist picrotoxin. Finally, both phases of the BPSP and the biphasic dopa mine response were desensitized by continuous bath application of dopamine. These results indicate that the biphasic RPeD1 --> VDI synapse is dopamine rgic. Collectively, these data suggest that the variability in sign (inhibi tory vs. biphasic) at the RPeD1 --> VD4 synapse is due to activation of two different dopamine receptors on the postsynaptic neuron VD4. This demonstr ates that two populations of receptors can produce two different forms of t ransmission, i.e., the inhibitory and biphasic forms of the single RPeD1 -- > VD4 synapse.