A circuit model of the temporal pattern generator of Caenorhabditis egg-laying behavior

Mi Zhang,Rainer Breitling,William R Schafer

doi:10.1186/1752-0509-4-81

Abstract

BackgroundEgg-laying behavior in the nematode C. elegans displays a distinct clustered temporal pattern: egg-laying events occur primarily in bursts or active phases, separated by inactive phases during which eggs are retained. The onset of the active phase can be modeled as a Poisson process with a time constant of approximately 20 minutes, while egg-laying events within an active phase occur with a faster time constant of approximately 20 seconds. Here we propose a cellular model for how the temporal pattern of egg-laying might be generated, based on genetic and cell-biological experiments and statistical analyses.ResultsWe suggest that the HSN neuron is the executive neuron driving egg-laying events. We propose that the VC neurons act as "single egg counters" that inhibit HSN activity for short periods in response to individual egg-laying events. We further propose that the uv1 neuroendocrine cells are "cluster counters", which inhibit HSN activity for longer periods and are responsible for the time constant of the inactive phase. Together they form an integrated circuit that drives the clustered egg-laying pattern.ConclusionsThe detailed predictions derived from this model can now be tested by straightforward validation experiments.

Highlights

Egg-laying behavior in the nematode C. elegans displays a distinct clustered temporal pattern: egg-laying events occur primarily in bursts or active phases, separated by inactive phases during which eggs are retained
In egl-15(n484) worms, which are defective in egg-laying behavior due to abnormal vulval muscle development, we found that half of HSN recordings exhibit unrestrained oscillations very similar to the theoretical pattern in Figure 2A, with HSN oscillating about half the time (4 out of 9 recordings) and silent otherwise (Figure 2C)
The cellular and molecular model we present here is the first one for generating a clustered pattern and so far the simplest to explain all available data, including our own extensive genetic manipulation results and behavior recordings

Summary

Introduction

Egg-laying behavior in the nematode C. elegans displays a distinct clustered temporal pattern: egg-laying events occur primarily in bursts or active phases, separated by inactive phases during which eggs are retained. We propose a cellular model for how the temporal pattern of egg-laying might be generated, based on genetic and cellbiological experiments and statistical analyses. The execution of specific behaviors relies on specialized motor programs, which generate specific spatial and temporal patterns of muscle contraction. The same logical regulatory structure can be used to control a wide variety of behavioral programs. This means that studying such pattern generating circuitries in experimental organisms can provide insights into fundamental circuit designs that are re-used in the much more complex brains of higher animals.

Methods

Results

Discussion

Conclusion