Dopamine Modulation of Phasing of Activity in a Rhythmic Motor Network: Contribution of Synaptic and Intrinsic Modulatory Actions

Abstract

The phasing of neuronal activity in a rhythmic motor network is determined by a neuron's intrinsic firing properties and synaptic inputs; these could vary in their relative importance under different modulatory conditions. In the lobster pyloric network, the firing of eight follower pyloric (PY) neurons is shaped by their intrinsic rebound after pacemaker inhibition and by synaptic input from the lateral pyloric (LP) neuron, which inhibits all PY neurons and is electrically coupled to a subset of them. Under control conditions, LP inhibition is weak and has little influence on PY firing. We examined modulation that could theoretically enhance the LP's synaptic contribution to PY firing. We measured the effects of dopamine (DA) on LP-->PY synapses, driving the LP neuron with trains of realistic waveforms constructed from prerecorded control and DA LP oscillations, which differed in shape and duration. Under control conditions, chemical inhibition underwent severe depression and disappeared; in the mixed synapses, electrical coupling dominated. Switching between control and DA LP waveforms (with or without DA present) caused only subtle changes in synaptic transmission. DA markedly enhanced synaptic inhibition, reduced synaptic depression and weakened electrical coupling, reversing the sign of the mixed synapses. Despite this, removal of the LP from the intact network still had only weak effects on PY firing. DA also enhances PY intrinsic rebound properties, which still control the onset of PY firing. Thus in a rhythmic network, the functional importance of synaptic modulation can only be understood in the context of parallel modulation of intrinsic properties.

Complex Intrinsic Membrane Properties and Dopamine Shape Spiking Activity in a Motor Axon

“…In H. americanus , the peripheral PD axon initiates spikes in response to low concentrations of DA (Bucher et al 2003a). DA has rich and diverse actions on virtually all identified voltage-dependent currents in the central compartments of STG neurons (Harris-Warrick et al, 1998; Kloppenburg et al, 1999; Peck et al, 2001; Johnson et al, 2003; Gruhn et al, 2005; Johnson et al, 2005; Peck et al, 2006). In the PD axons, it predominantly seems to act by increasing I H (Fig.…”

Neuromodulation of neurons and synapses

“…In the STG, the inhibitory synaptic connection from one follower neuron to another is strengthened by dopamine without changing its influence on the postsynaptic activity [31]. In the same system, the inhibitory feedback connection from a follower neuron to pacemaker neurons is greatly strengthened by two neuropeptides [32,33 • ] with no apparent consequence for network frequency.…”

Peptide Neuromodulation of Synaptic Dynamics in an Oscillatory Network

“…The sole chemical feedback from the pyloric follower neurons to the pacemakers is the synapse from the lateral pyloric (LP) to the PD neurons, according a key role for this synapse in the regulation of pyloric oscillations (Manor et al, 1997; Mamiya et al, 2003; Weaver and Hooper, 2003). A variety of neuromodulators in the STNS modify the intrinsic properties of individual pyloric neurons (Harris-Warrick et al, 1998; Swensen and Marder, 2000) and the strength and dynamics of synapses among these neurons (Johnson et al, 2005; Johnson et al, 2011). We demonstrate the ability of the modulatory neuropeptide proctolin to alter the strength and unmask novel dynamics in the LP to PD synapse.…”