Dopamine-induced oscillations of the pyloric pacemaker neuron rely on release of calcium from intracellular stores

Abstract

Kadiri LR, Kwan AC, Webb WW, Harris-Warrick RM. Dopamineinduced oscillations of the pyloric pacemaker neuron rely on release of calcium from intracellular stores. J Neurophysiol 106: 1288-1298, 2011. First published June 15, 2011 doi:10.1152/jn.00456.2011.-Endogenously bursting neurons play central roles in many aspects of nervous system function, ranging from motor control to perception. The properties and bursting patterns generated by these neurons are subject to neuromodulation, which can alter cycle frequency and amplitude by modifying the properties of the neuron's ionic currents. In the stomatogastric ganglion (STG) of the spiny lobster, Panulirus interruptus, the anterior burster (AB) neuron is a conditional oscillator in the presence of dopamine (DA) and other neuromodulators and serves as the pacemaker to drive rhythmic output from the pyloric network. We analyzed the mechanisms by which DA evokes bursting in the AB neuron. Previous work showed that DA-evoked bursting is critically dependent on external calcium (Harris-Warrick RM, Flamm RE. J Neurosci 7: [2113][2114][2115][2116][2117][2118][2119][2120][2121][2122][2123][2124][2125][2126][2127][2128] 1987). Using two-photon microscopy and calcium imaging, we show that DA evokes the release of calcium from intracellular stores well before the emergence of voltage oscillations. When this release from intracellular stores is blocked by antagonists of ryanodine or inositol trisphosphate (IP 3 ) receptor channels, DA fails to evoke AB bursting. We further demonstrate that DA enhances the calcium-activated inward current, I CAN , despite the fact that it significantly reduces voltage-activated calcium currents. This suggests that DA-induced release of calcium from intracellular stores activates I CAN , which provides a depolarizing ramp current that underlies endogenous bursting in the AB neuron.calcium-activated inward current; ryanodine; voltage clamp; central pattern generator RHYTHMIC ACTIVITY plays central roles in many aspects of nervous system function, ranging from motor control to perception. The neural mechanisms underlying rhythmogenesis are not well understood but include both network-driven oscillators and neuronal oscillators (Harris-Warrick 2010). Neuronal oscillators are single neurons that generate an endogenous oscillatory voltage pattern based on the ionic currents they express. The bursting properties of these neurons are subject to neuromodulation, which can alter cycle frequency and amplitude by modifying the properties of the neuron's ionic currents (Harris-Warrick and Johnson 2010;Lotshaw et al. 1986;Marder and Bucher 2001;Marder et al. 2005;Partridge et al. 1990).The pyloric network in the crustacean stomatogastric ganglion (STG) is an important system for studying the mechanisms of rhythmogenesis (Harris-Warrick 1993; Marder and Bucher 2001; Selverston and Ayers 2006). The pyloric circuit consists of 1 interneuron (the anterior burster, or AB) and 13 motoneurons. The AB neuron is a conditional oscillator: under the appropriate modul...

Implication of dopaminergic modulation in operant reward learning and the induction of compulsive-like feeding behavior inAplysia

“…increases the excitability and stabilizes the intrinsic oscillatory properties of the buccal pattern-initiating B63 neurons, and, as a result, is able to reproduce essential features of the cellular plasticity resulting from behavioral associative learning (Nargeot et al 2009). DA has been previously found capable of activating endogenous oscillatory mechanisms in previously silent neurons or increasing the frequency of ongoing oscillatory activity (Flamm and Harris-Warrick 1986b;Kadiri et al 2011). Our data extend these findings by showing that the amine can also regularize the otherwise erratic expression of neuronal oscillatory activity, thereby leading to stereotyped rhythmic bursting (see also Serrano and Miller 2006).…”

Activation of high and low affinity dopamine receptors generates a closed loop that maintains a conductance ratio and its activity correlate

“…Interestingly, LP I h G max did not change over time in 5 nM DA preparations where slow wave activity was mimicked (paired t -test, t = 0 vs. 10 min, p = 0.5962); however, a complete block of activity produced a clear trend toward an increase in LP I h G max (paired t -test, p = 0.0596), and the magnitude of the increase was similar to that observed in 5 μM DA (compare Figures 2B vs. 2E). The difference in the TTX + OSC treatment groups in 5 nM DA (no change in G max ) vs. 5 μM DA (decrease in G max ) may be due to the fact that micromolar DA can regulate calcium dynamics during oscillations in membrane potential (Johnson et al, 2003; Kadiri et al, 2011). For all treatment groups the voltages of half activation changed by ≤2.3 mV on average, and LP I h voltage dependence is not considered further here.…”

“…It is tempting to speculate that the mechanism(s) that is sensitive to burst duration and cycle frequency senses Ca 2 + release from stores while the mechanism(s) that is sensitive to spiking senses Ca 2 + entry through voltage-gated calcium channels. It was previously noted that Ca 2 + release from stores can regulate I h density in hippocampal neurons (Narayanan et al, 2010), and that in the pyloric AB neuron, Ca 2 + release oscillates with oscillations in membrane potential (Kadiri et al, 2011). Thus, changes in cycle frequency and burst duration could alter steady-state Ca 2 + contributed by store release.…”

The mitochondrial Na+-Ca2+ exchanger, NCLX, regulates automaticity of HL-1 cardiomyocytes

“…For example, the initiation of pacemaker activity in the interstitial Cajal cell, which is a pacemaker cell in the gastrointestinal tract and fallopian tubes, is caused by release of ER/SR Ca 2+ through inositol 1,4,5-trisphosphate receptor and/or RyR channel5354. In addition, recent findings suggest that Ca 2+ release from ER via RyR channels are involved in the firing of neurons5556. NCLX might also supply Ca 2+ to ER/SR of these cells, thus contributing to making rhythmicity.…”