Tonic Dopamine Induces Persistent Changes in the Transient Potassium Current through Translational Regulation

Rodgers, Edmund W.; Krenz, Wulf-Dieter C.; Baro, Deborah J.

doi:10.1523/jneurosci.2194-11.2011

Cited by 21 publications

(45 citation statements)

References 75 publications

(125 reference statements)

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“…Experimental and computational studies suggest that distinct conductance ratios are maintained in identified pyloric neurons, including the ratio of LP I A to I h (Schulz et al, 2006(Schulz et al, , 2007Hudson and Prinz, 2010), and modulators are necessary for their maintenance (Khorkova and Golowasch, 2007). Interestingly, steadystate DA also regulates LP I A G max (Rodgers et al, 2011).…”

Section: Discussionmentioning

confidence: 99%

“…By convention the first spike in the pyloric dilator neuron (PD) defines the beginning of a pyloric cycle, and the phasing of pyloric neurons is determined relative to the start of the cycle. Since we were interested in recovery mechanisms intrinsic to LP, we broke with convention and used the last spike in PD to define the beginning of the cycle, because tonic DA can cause persistent changes in PD ionic conductances (Rodgers et al, 2011). One cycle period was therefore defined as the last spike in one PD burst to the last spike in the next PD burst (Fig.…”

Section: Methodsmentioning

confidence: 99%

“…Depletion of Ca 2ϩ stores and a concomitant increase in cytosolic Ca 2ϩ can also increase HCN surface expression perisomatically . We have previously shown that steady-state nanomolar DA can regulate LP I A G max through a translation-dependent, activityindependent mechanism mediated by target of rapamycin (TOR) (Rodgers et al, 2011). Reductions in LP burst duration may modulate this pathway.…”

Section: Phase Homeostasis?mentioning

confidence: 99%

“…Phasic and tonic dopamine (DA) transmissions have distinct functions (Schultz, 2007): phasic release encodes temporally relevant information and modifies neuronal function on a moment-to-moment basis, while steady-state or tonic DA in the extracellular space is thought to enable motor and cognitive processes. Tonic nanomolar DA can act through translation-dependent mechanisms to persistently regulate the voltage-gated transient potassium current (I A ) in an activityindependent fashion (Rodgers et al, 2011). A recent study showed that diminished dopaminergic tone in mouse models of Parkinson's disease caused a loss of pacemaker activity and a reduction in I h in globus pallidus neurons (Chan et al, 2011).…”

Section: Introductionmentioning

confidence: 99%

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Tonic Nanomolar Dopamine Enables an Activity-Dependent Phase Recovery Mechanism That Persistently Alters the Maximal Conductance of the Hyperpolarization-Activated Current in a Rhythmically Active Neuron

Rodgers

Fu²,

Krenz³

et al. 2011

J. Neurosci.

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The phases at which network neurons fire in rhythmic motor outputs are critically important for the proper generation of motor behaviors. The pyloric network in the crustacean stomatogastric ganglion generates a rhythmic motor output wherein neuronal phase relationships are remarkably invariant across individuals and throughout lifetimes. The mechanisms for maintaining these robust phase relationships over the long-term are not well described. Here we show that tonic nanomolar dopamine (DA) acts at type 1 DA receptors (D1Rs) to enable an activity-dependent mechanism that can contribute to phase maintenance in the lateral pyloric (LP) neuron. The LP displays continuous rhythmic bursting. The activity-dependent mechanism was triggered by a prolonged decrease in LP burst duration, and it generated a persistent increase in the maximal conductance (G max ) of the LP hyperpolarization-activated current (I h ), but only in the presence of steady-state DA. Interestingly, micromolar DA produces an LP phase advance accompanied by a decrease in LP burst duration that abolishes normal LP network function. During a 1 h application of micromolar DA, LP phase recovered over tens of minutes because, the activity-dependent mechanism enabled by steady-state DA was triggered by the micromolar DA-induced decrease in LP burst duration. Presumably, this mechanism restored normal LP network function. These data suggest steady-state DA may enable homeostatic mechanisms that maintain motor network output during protracted neuromodulation. This DA-enabled, activitydependent mechanism to preserve phase may be broadly relevant, as diminished dopaminergic tone has recently been shown to reduce I h in rhythmically active neurons in the mammalian brain.

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Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Phase Homeostasis?mentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Tonic Nanomolar Dopamine Enables an Activity-Dependent Phase Recovery Mechanism That Persistently Alters the Maximal Conductance of the Hyperpolarization-Activated Current in a Rhythmically Active Neuron

Rodgers

Fu²,

Krenz³

et al. 2011

J. Neurosci.

Self Cite

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show abstract

“…cAMP/protein kinase A signaling has been found to be important for DA to modulate I A in LP neurons (Zhang et al, 2010). Additionally, this K current has been shown to be enhanced by tonic stimulation with nanomolar DA concentration through a translationdependent mechanism involving the target of rapamycin pathway in crustacean LP neurons (Rodgers et al, 2011), a process thought to dampen extrinsic excitatory inputs.…”

Section: Ion Channels Modulated By Damentioning

confidence: 99%

Dopamine suppresses neuronal activity of Helisoma B5 neurons via a D2-like receptor, activating PLC and K channels

2013

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Molecular mechanisms of homeostatic plasticity in central pattern generator networks

Northcutt

Schulz

2019

Developmental Neurobiology

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Central pattern generator (CPG) networks rely on a balance of intrinsic and network properties to produce reliable, repeatable activity patterns. This balance is maintained by homeostatic plasticity where alterations in neuronal properties dynamically maintain appropriate neural output in the face of changing environmental conditions and perturbations. However, it remains unclear just how these neurons and networks can both monitor their ongoing activity and use this information to elicit homeostatic physiological responses to ensure robustness of output over time. Evidence exists that CPG networks use a mixed strategy of activity‐dependent, activity‐independent, modulator‐dependent, and synaptically regulated homeostatic plasticity to achieve this critical stability. In this review, we focus on some of the current understanding of the molecular pathways and mechanisms responsible for this homeostatic plasticity in the context of central pattern generator function, with a special emphasis on some of the smaller invertebrate networks that have allowed for extensive cellular‐level analyses that have brought recent insights to these questions.

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Tonic Dopamine Induces Persistent Changes in the Transient Potassium Current through Translational Regulation

Cited by 21 publications

References 75 publications

Tonic Nanomolar Dopamine Enables an Activity-Dependent Phase Recovery Mechanism That Persistently Alters the Maximal Conductance of the Hyperpolarization-Activated Current in a Rhythmically Active Neuron

Tonic Nanomolar Dopamine Enables an Activity-Dependent Phase Recovery Mechanism That Persistently Alters the Maximal Conductance of the Hyperpolarization-Activated Current in a Rhythmically Active Neuron

Dopamine suppresses neuronal activity of Helisoma B5 neurons via a D2-like receptor, activating PLC and K channels

Molecular mechanisms of homeostatic plasticity in central pattern generator networks

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