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

BackgroundCrustaceans have been studied extensively as model systems for nervous system function from single neuron properties to behavior. However, lack of molecular sequence information and tools have slowed the adoption of these physiological systems as molecular model systems. In this study, we sequenced and performed de novo assembly for the nervous system transcriptomes of two decapod crustaceans: the Jonah crab (Cancer borealis) and the American lobster (Homarus americanus).ResultsForty-two thousand, seven hundred sixty-six and sixty thousand, two hundred seventy-three contigs were assembled from C. borealis and H. americanus respectively, representing 9,489 and 11,061 unique coding sequences. From these transcripts, genes associated with neural function were identified and manually curated to produce a characterization of multiple gene families important for nervous system function. This included genes for 34 distinct ion channel types, 17 biogenic amine and 5 GABA receptors, 28 major transmitter receptor subtypes including glutamate and acetylcholine receptors, and 6 gap junction proteins – the Innexins.ConclusionWith this resource, crustacean model systems are better poised for incorporation of modern genomic and molecular biology technologies to further enhance the interrogation of fundamentals of nervous system function.

The dynamics of neuronal firing during natural vision are poorly understood. Surprisingly, mean firing rates of neurons in primary visual cortex (V1) of freely behaving rodents are similar during prolonged periods of light and darkness, but it is unknown whether this reflects a slow adaptation to changes in natural visual input or insensitivity to rapid changes in visual drive. Here, we use chronic electrophysiology in freely behaving rats to follow individual V1 neurons across many dark–light (D-L) and light–dark (L-D) transitions. We show that, even on rapid timescales (1 s to 10 min), neuronal activity was only weakly modulated by transitions that coincided with the expected 12-/12-h L-D cycle. In contrast, a larger subset of V1 neurons consistently responded to unexpected L-D and D-L transitions, and disruption of the regular L-D cycle with 60 h of complete darkness induced a robust increase in V1 firing on reintroduction of visual input. Thus, V1 neurons fire at similar rates in the presence or absence of natural stimuli, and significant changes in activity arise only transiently in response to unexpected changes in the visual environment. Furthermore, although mean rates were similar in light and darkness, pairwise correlations were significantly stronger during natural vision, suggesting that information about natural scenes in V1 may be more strongly reflected in correlations than individual firing rates. Together, our findings show that V1 firing rates are rapidly and actively stabilized during expected changes in visual input and are remarkably stable at both short and long timescales.

Plasticity of excitability can come in two general forms: changes in excitability that alter neuronal output (e.g. long-term potentiation of intrinsic excitability) or excitability changes that stabilize neuronal output (homeostatic plasticity). Here we discuss the latter form of plasticity in the context of the crustacean stomatogastric nervous system, and a second central pattern generator circuit, the cardiac ganglion. We discuss this plasticity at three levels: rapid homeostatic changes in membrane conductance, longer-term effects of neuromodulation on excitability, and the impacts of activity-dependent feedback on steady-state channel mRNA levels. We then conclude with thoughts on the implications of plasticity of excitability for variability of conductance levels across populations of motor neurons.

The Large Cell (LC) motor neurons of the crab cardiac ganglion have variable membrane conductance magnitudes even within the same individual, yet produce identical synchronized activity in the intact network. In a previous study we blocked a subset of K+ conductances across LCs, resulting in loss of synchronous activity (Lane et al., 2016). In this study, we hypothesized that this same variability of conductances makes LCs vulnerable to desynchronization during neuromodulation. We exposed the LCs to serotonin (5HT) and dopamine (DA) while recording simultaneously from multiple LCs. Both amines had distinct excitatory effects on LC output, but only 5HT caused desynchronized output. We further determined that DA rapidly increased gap junctional conductance. Co-application of both amines induced 5HT-like output, but waveforms remained synchronized. Furthermore, DA prevented desynchronization induced by the K+ channel blocker tetraethylammonium (TEA), suggesting that dopaminergic modulation of electrical coupling plays a protective role in maintaining network synchrony.