Abstract
Long-term intrinsic and synaptic plasticity must be coordinated to ensure stability and flexibility in neuronal circuits. Coordination might be achieved through shared transduction components. Dopamine (DA) is a well-established participant in many forms of long-term synaptic plasticity. Recent work indicates that DA is also involved in both activity-dependent and -independent forms of long-term intrinsic plasticity. We previously examined DA-enabled long-term intrinsic plasticity in a single identified neuron. The lateral pyloric (LP) neuron is a component of the pyloric network in the crustacean stomatogastric nervous system (STNS). LP expresses type 1 DA receptors (D1Rs). A 1 h bath application of 5 nM DA followed by washout produced a significant increase in the maximal conductance (Gmax) of the LP transient potassium current (IA) that peaked ~4 h after the start of DA application; furthermore, if a change in neuronal activity accompanied the DA application, then a persistent increase in the LP hyperpolarization activated current (Ih) was also observed. Here, we repeated these experiments with pharmacological and peptide inhibitors to determine the cellular processes and signaling proteins involved. We discovered that the persistent, DA-induced activity-independent (IA) and activity-dependent (Ih) changes in ionic conductances depended upon many of the same elements that enable long-term synaptic plasticity, including: the D1R-protein kinase A (PKA) axis, RNA polymerase II transcription, RNA interference (RNAi), and mechanistic target of rapamycin (mTOR)-dependent translation. We interpret the data to mean that increasing the tonic DA concentration enhances expression of a microRNA(s) (miRs), resulting in increased cap-dependent translation of an unidentified protein(s).
Highlights
Dopaminergic systems use volume transmission to modulate cognitive and motor functions (Zoli et al, 1998; Schultz, 2007; Oginsky et al, 2010)
We previously showed that the sole lateral pyloric (LP) neuron in the stomatogastric nervous system (STNS) of the spiny lobster, Panulirus interruptus, expressed high and low affinity D1Rs but not D2Rs (Zhang et al, 2010; Rodgers et al, 2011a,b; Krenz et al, 2013)
THE SAME SLOW PROCESSES ARE NECESSARY FOR THE 5 nM DA INDUCED, ACTIVITY-INDEPENDENT INCREASE IN LATERAL PYLORIC (LP) I h G max far we have examined the cellular processes underpinning the persistent increase in LP Ih Gmax without regard for other voltage-gated ionic conductances; LP IA and Ih can be co-regulated (MacLean et al, 2005; Temporal et al, 2012; Krenz et al, 2013)
Summary
Dopaminergic systems use volume transmission to modulate cognitive and motor functions (Zoli et al, 1998; Schultz, 2007; Oginsky et al, 2010). Tonic and burst firing neurons release Dopamine (DA) that can diffuse and act predominantly at remote extra-synaptic receptors before reuptake by DA transporters. Phasic DA may encode reward prediction error (Steinberg et al, 2013), provide sustained motivational drive (Howe et al, 2013) and modulate motor behaviors (Gerfen and Surmeier, 2011). Tonic DA is thought to have an enabling function because tonic administration of drugs, such as L-dopa or neuroleptics, can enable motor, motivational and cognitive behaviors (Schultz, 2007). The effects of tonic DA have largely been attributed to D2Rs, but all receptors can show high and low affinity states and there is increasing evidence that tonic DA acting at high affinity type 1 DA receptors (D1Rs) may enable and shape circuit output over the long-term (Trantham-Davidson et al, 2004; Rodgers et al, 2011a,b; Wall et al, 2011; Saba et al, 2012)
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