Animal behaviors are commonly organized into long-lasting states that coordinately impact the generation of diverse motor outputs such as feeding, locomotion, and grooming. However, the neural mechanisms that coordinate these distinct motor programs remain poorly understood. Here, we examine how the distinct motor programs of the nematode C. elegans are coupled together across behavioral states. We describe a new imaging platform that permits automated, simultaneous quantification of each of the main C. elegans motor programs over hours or days. Analysis of these whole-organism behavioral profiles shows that the motor programs coordinately change as animals switch behavioral states. Utilizing genetics, optogenetics, and calcium imaging, we identify a new role for dopamine in coupling locomotion and egg-laying together across states. These results provide new insights into how the diverse motor programs throughout an organism are coordinated and suggest that neuromodulators like dopamine can couple motor circuits together in a state-dependent manner.
Keywords: C. elegans; behavioral states; c elegans; dopamine; motor programs; neural circuits; neuromodulation; neuroscience.
Animals generate many different motor programs (such as moving, feeding and grooming) that they can alter in response to internal needs and environmental cues. These motor programs are controlled by dedicated brain circuits that act on specific muscle groups. However, little is known about how organisms coordinate these different motor programs to ensure that their resulting behavior is coherent and appropriate to the situation. This is difficult to investigate in large organisms with complex nervous systems, but with 302 brain cells that control 143 muscle cells, the small worm Caenorhabditis elegans provides a good system to examine this question. Here, Cermak, Yu, Clark et al. devised imaging methods to record each type of motor program in C. elegans worms over long time periods, while also dissecting the underlying neural mechanisms that coordinate these motor programs. This constitutes one of the first efforts to capture and quantify all the behavioral outputs of an entire organism at once. The experiments also showed that dopamine – a messenger molecule in the brain – links the neural circuits that control two motor programs: movement and egg-laying. A specific type of high-speed movement activates brain cells that release dopamine, which then transmits this information to the egg-laying circuit. This means that worms lay most of their eggs whilst traveling at high speed through a food source, so that their progeny can be distributed across a nutritive environment. This work opens up the possibility to study how behaviors are coordinated at the level of the whole organism – a departure from the traditional way of focusing on how specific neural circuits generate specific behaviors. Ultimately, it will also be interesting to look at the role of dopamine in behavior coordination in a wide range of animals.
© 2020, Cermak et al.