Dopamine Modulates Two Potassium Currents and Inhibits the Intrinsic Firing Properties of an Identified Motor Neuron in a Central Pattern Generator Network

Abstract

The two pyloric dilator (PD) neurons are components [along with the anterior burster (AB) neuron] of the pacemaker group of the pyloric network in the stomatogastric ganglion of the spiny lobster Panulirus interruptus. Dopamine (DA) modifies the motor pattern generated by the pyloric network, in part by exciting or inhibiting different neurons. DA inhibits the PD neuron by hyperpolarizing it and reducing its rate of firing action potentials, which leads to a phase delay of PD relative to the electrically coupled AB and a reduction in the pyloric cycle frequency. In synaptically isolated PD neurons, DA slows the rate of recovery to spike after hyperpolarization. The latency from a hyperpolarizing prestep to the first action potential is increased, and the action potential frequency as well as the total number of action potentials are decreased. When a brief (1 s) puff of DA is applied to a synaptically isolated, voltage-clamped PD neuron, a small voltage-dependent outward current is evoked, accompanied by an increase in membrane conductance. These responses are occluded by the combined presence of the potassium channel blockers 4-aminopyridine and tetraethylammonium. In voltage-clamped PD neurons, DA enhances the maximal conductance of a voltage-sensitive transient potassium current (IA) and shifts its Vact to more negative potentials without affecting its Vinact. This enlarges the "window current" between the voltage activation and inactivation curves, increasing the tonically active IA near the resting potential and causing the cell to hyperpolarize. Thus DA's effect is to enhance both the transient and resting K+ currents by modulating the same channels. In addition, DA enhances the amplitude of a calcium-dependent potassium current (IO(Ca)), but has no effect on a sustained potassium current (IK(V)). These results suggest that DA hyperpolarizes and phase delays the activity of the PD neurons at least in part by modulating their intrinsic postinhibitory recovery properties. This modulation appears to be mediated in part by an increase of IA and IO(Ca). IA appears to be a common target of DA action in the pyloric network, but it can be enhanced or decreased in different ways by DA in different neurons.

Arthropod D2 receptors positively couple with cAMP through the Gi/o protein family

“…The effects of DA on a model CPG, the pyloric network, have been extremely well characterized (Harris-Warrick et al, 1998;Gruhn et al, 2005;Johnson et al, 2003;Kloppenburg et al, 2000;Kloppenburg et al, 1999;Peck et al, 2001); however, the molecular mechanisms by which DA exerts its effects are completely unknown. To begin to investigate the molecular underpinnings of the dopaminergic response in pyloric neurons, we cloned and characterized the only known arthropod type-2 DAR from Panulirus interruptus: D 2αPan .…”

“…A wealth of information exists on the monoaminergic modulation of ion currents and neuronal firing properties (Flamm and Harris-Warrick, 1986;HarrisWarrick et al, 1995b;Harris-Warrick et al, 1995a;Harris-Warrick et al, 1998;Kloppenburg et al, 1999;Johnson et al, 2003), but nothing is known about the transduction cascades mediating these effects. To extend the usefulness of this model system and gain insight into how component neurons integrate biochemical and electrical processes, we have begun a molecular characterization of DARs in this central pattern generator (CPG).…”

Multiple Peptides Converge to Activate the Same Voltage-Dependent Current in a Central Pattern-Generating Circuit

“…The stomatogastric nervous system contains ϳ20 different identified modulatory substances (Marder and Weimann, 1992;Marder et al, 1995;Christie et al, 1997a;Abbott and Marder, 1998), each of which can alter the STG motor patterns. The effects of serotonin (Kiehn and HarrisWarrick, 1992a,b;Zhang and Harris-Warrick, 1995), dopamine (Harris-Warrick et al, 1995a,b;Kloppenburg et al, 1999), and the peptide proctolin (Golowasch and Marder, 1992) have been characterized, but until now, the biophysical actions of most of the modulatory substances found in inputs to the STG were unknown.…”

“…Additionally, in low external calcium the current-voltage curve for the proctolin-induced current linearizes. Serotonin and dopamine modulate several of the voltage-gated currents in STG neurons (Kiehn and HarrisWarrick, 1992a,b; Harris-Warrick et al, 1995a,b;Zhang and Harris-Warrick, 1995;Kloppenburg et al, 1999).In this paper we study the effects of six neuromodulators [proctolin, Cancer borealis tachykinin-related peptide Ia (CabTRP), crustacean cardioactive peptide (CCAP), red pigment-concentrating hormone (RPCH), TNRNFLRFamide, and the muscarinic agonist pilocarpine]. These modulators all have excitatory effects at the network level and are able to activate the pyloric rhythm in quiescent preparations (Hooper and Marder, 1984;Marder and Hooper, 1985;Nusbaum and Marder, 1988;Weimann et al, 1993Weimann et al, , 1997Christie et al, 1997b).…”

“…Additionally, in low external calcium the current-voltage curve for the proctolin-induced current linearizes. Serotonin and dopamine modulate several of the voltage-gated currents in STG neurons (Kiehn and HarrisWarrick, 1992a,b; Harris-Warrick et al, 1995a,b;Zhang and Harris-Warrick, 1995;Kloppenburg et al, 1999).…”