Activity of the C. elegans egg-laying behavior circuit is controlled by competing activation and feedback inhibition

Abstract

Like many behaviors, Caenorhabditis elegans egg laying alternates between inactive and active states. To understand how the underlying neural circuit turns the behavior on and off, we optically recorded circuit activity in behaving animals while manipulating circuit function using mutations, optogenetics, and drugs. In the active state, the circuit shows rhythmic activity phased with the body bends of locomotion. The serotonergic HSN command neurons initiate the active state, but accumulation of unlaid eggs also promotes the active state independent of the HSNs. The cholinergic VC motor neurons slow locomotion during egg-laying muscle contraction and egg release. The uv1 neuroendocrine cells mechanically sense passage of eggs through the vulva and release tyramine to inhibit egg laying, in part via the LGC-55 tyramine-gated Cl- channel on the HSNs. Our results identify discrete signals that entrain or detach the circuit from the locomotion central pattern generator to produce active and inactive states.DOI: http://dx.doi.org/10.7554/eLife.21126.001

Local neuropeptide signaling modulates serotonergic transmission to shape the temporal organization of C. elegans egg-laying behavior

“…Prior work suggested that the neurosecretory uv1 cells may terminate egg-laying, perhaps by sensing the passage of eggs through the vulva [18,29]. Our work supports this model and extends it in several important aspects.…”

“…Prolonged inhibition of the uv1 cells in adult animals significantly reduces the length of the inactive phase of egg-laying. A recent study found that calcium transients occur in uv1 cells immediately following egg-laying events during an active phase [18], suggesting that repetitive stimulation of uv1 cells may be required for inhibition of egg-laying. We speculate that each egg-laying event may trigger release from the uv1 cells, ultimately leading to local increases in peptide levels sufficient to terminate the active phase and delay re-entry into the subsequent active phase.…”

“…elegans egg-laying behavior cycles probabilistically between two alternative states: active phases containing short bursts of egg-laying and prolonged periods of quiescence (inactive phases) [9,18–20]. This temporal organization of egg-laying allows for spatial dispersal of eggs, and may be beneficial for survival of progeny by limiting local overcrowding and competition for food.…”

High-Content Microfluidic Screening Platform Used To Identify σ2R/Tmem97 Binding Ligands that Reduce Age-Dependent Neurodegeneration in C. elegans SC_APP Model

“…Calcium transients in VC neurons, particularly VC4 and 5, are temporally associated with egg laying events. 42 Thus, we analyzed egg laying behavior to determine if behavioral differences could be used to screen for neuroprotective treatments. Consistent with a recent report of silencing VC neuron activity that did not alter the number of unlaid eggs, 43 we found no difference in the average number of unlaid eggs on D1 or D3 of adulthood for SC_APP and WT worms (Figure 2a).…”

“…42 We first tested whether VC neuron ablation by cell-specific expression of human Casp1 (ICE) impaired swimming. As similar results were found for head bend rate and swim speed, only swim speed is reported.…”