Rapid Dopaminergic Signaling by Interneurons That Contain Markers for Catecholamines and GABA in the Feeding Circuitry of Aplysia

Abstract

Consummatory feeding behaviors in Aplysia californica are controlled by a polymorphic central pattern generator (CPG) circuit. Previous investigations have demonstrated colocalization of markers for GABA and catecholamines within two interneurons, B20 and B65, that participate in configuring the functional output of this CPG. This study examined the contributions of GABA and dopamine (DA) to rapid synaptic signaling from B20 and B65 to follower cells that implement their specification of motor programs. Pharmacological tests did not substantiate the participation of GABA in the mediation of the excitatory postsynaptic potentials (EPSPs) from either B20 or B65. However, GABA and the GABA(B) receptor agonist baclofen were found to modify these signals in a target-specific manner. Several observations indicated that DA acts as the neurotransmitter mediating fast EPSPs from B20 to two radula closer motor neurons B8 and B16. In both motor neurons, application of DA produced depolarizing responses associated with decreased input resistance and increased excitation. B20-evoked EPSPs in both follower cells were occluded by exogenous dopamine and blocked by the DA antagonist sulpiride. While dopamine occlusion and sulpiride block of convergent signaling to B8 from B65 resembled that of B20, both of these actions were less potent on the rapid signaling from B65 to the multifunctional and widely acting interneuron B4/5. These findings indicate that dopamine mediates divergent (B20 to B16 and B8) and convergent (B20 and B65 to B8) rapid EPSPs from two influential CPG interneurons in which it is colocalized with GABA-like immunoreactivity.

PKC-mediated GABAergic enhancement of dopaminergic responses: implication for short-term potentiation at a dual-transmitter synapse

“…Dopamine-evoked fast inward currents in B8 reversed at ϳ0 mV, indicating that nonselective cation channels are involved ( Fig. 2A; n ϭ 3) as previously suggested (Díaz-Ríos and Miller 2005).…”

“…Dopamine acts as a fast transmitter at the B20 synapse with the feeding motoneuron B8. Although GABA does not elicit any fast PSPs at this synapse, it can potentiate the dopaminergic EPSPs elicited in B8 (Díaz-Ríos and Miller 2005). However, the sites and mechanisms of GABA action at this synapse remain unknown.…”

“…Previous experiments (e.g., Díaz-Ríos and Miller 2005) demonstrated that the dopaminergic EPSPs elicited by B20 in B8 were potentiated when GABA was exogenously applied, but the mechanisms of this action remained uncharacterized. Here, we sought to determine whether GABA can elicit the potentiation in the presence of TTX to minimize the possibility of polysynaptic effects.…”

“…Previous work showed that fast dopamine responses in Aplysia can be blocked by sulpiride (Díaz-Ríos and Miller 2005;Due et al 2004). This effect is unexpected as sulpiride is considered a D 2 -receptor antagonist.…”

“…We investigated the pharmacological profile of the receptor through which GABA acts on B8 to facilitate dopamine-evoked currents. We examined the effects of the GABA B -receptor agonist baclofen, which increases the size of B20-to-B8 EPSPs (Díaz-Ríos and Miller 2005). Baclofen (100 M) mimicked the action of GABA, as it potentiated dopamine currents to 168.4 Ϯ 29.2% of control ( Fig.…”