Synergistic plasticity of intrinsic conductance and electrical coupling restores synchrony in an intact motor network

Abstract

Motor neurons of the crustacean cardiac ganglion generate virtually identical, synchronized output despite the fact that each neuron uses distinct conductance magnitudes. As a result of this variability, manipulations that target ionic conductances have distinct effects on neurons within the same ganglion, disrupting synchronized motor neuron output that is necessary for proper cardiac function. We hypothesized that robustness in network output is accomplished via plasticity that counters such destabilizing influences. By blocking high-threshold K+ conductances in motor neurons within the ongoing cardiac network, we discovered that compensation both resynchronized the network and helped restore excitability. Using model findings to guide experimentation, we determined that compensatory increases of both GA and electrical coupling restored function in the network. This is one of the first direct demonstrations of the physiological regulation of coupling conductance in a compensatory context, and of synergistic plasticity across cell- and network-level mechanisms in the restoration of output.DOI: http://dx.doi.org/10.7554/eLife.16879.001

Simple models of quantitative firing phenotypes in hippocampal neurons: comprehensive coverage of intrinsic diversity

“…While Hebbian plasticity rules can enable flexible ranges in synaptic conductances, the rules governing a neuron's intrinsic plasticity remain largely unknown. Although cell-autonomous regulatory rules have been proposed [47], 510 from a network perspective, intrinsic homeostasis have been shown to synergistically result from multiple interacting components in a circuit [48,49]. Exhaustively reductionist approaches to modeling brain regions specify precise descriptions at the level of ion channel conductances.…”

Homeostatic plasticity of excitability in crustacean central pattern generator networks

“…Further, due to intrinsic variability across LCs, TEA causes LCs to lose conserved output and produce divergent voltage responses [19], and in an ongoing network rhythm LC burst waveforms become desynchronized. Synchrony is then restored within 1 hour via at least 2 conductance changes acting synergistically [19,20]. The compensatory increase in I A contributes to resynchronization, along with a compensatory increase in electrical coupling among LCs [20].…”

“…Synchrony is then restored within 1 hour via at least 2 conductance changes acting synergistically [19,20]. The compensatory increase in I A contributes to resynchronization, along with a compensatory increase in electrical coupling among LCs [20]. …”

Dopamine maintains network synchrony via direct modulation of gap junctions in the crustacean cardiac ganglion

“…The crustacean cardiac ganglion (CG) is a central pattern generator network that produces rhythmic bursts with precisely synchronized activity across all five Large Cell (LC) motor neurons ( Lane et al, 2016 ), constituent LCs are variable in many ionic conductances, including A-type K+ (IA), high-threshold K+ (IHTK), and voltage-dependent Ca2+ (ICa) ( Ransdell et al, 2013a , b; Lane et al, 2016 ). When subsets of K+ conductances are blocked in LCs of a network, synchrony is disrupted, although ultimately is restored by a combination compensatory changes in membrane conductance and electrical synaptic strength ( Lane et al, 2016 ).…”

“… Abstract Abstract The Large Cell (LC) motor neurons of the crab (C. borealis) cardiac ganglion have variable membrane conductance magnitudes even within the same individual, yet produce identical synchronized activity in the intact network. In our previous study ( Lane et al, 2016 ) we blocked a subset of K + conductances across LCs, resulting in loss of synchronous activity. In this study, we hypothesized that this same variability of conductances could make LCs vulnerable to desynchronization during neuromodulation.…”