Whole-organism behavioral profiling reveals a role for dopamine in state-dependent motor program coupling in C. elegans

Abstract

<jats:p>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.</jats:p>

Behavioral States

“…In contrast, dopaminergic neurons are thought to be activated by the presence of bacterial food and the release of dopamine controls the animal's roaming speed (Sawin et al 2000;Stern et al 2017). In addition, dopamine release during roaming increases the animal's egg-laying rate, so that animals display higher egg-laying rates during roaming vs. dwelling, which allows them to disperse their eggs across a food source (Cermak et al 2020). The fact that multiple biogenic amines and neuropeptides are required for the proper expression of roaming and dwelling states suggests that these states are specified by the combinatorial action of many neuromodulators.…”

Host-microbe interactions and the behavior of Caenorhabditis elegans

“…daf-7 expression in ASJ is also positively regulated by satiety, thus allowing it to serve as a signal that integrates multiple internal cues to promote exploration. Increased motion through bacterial lawns during roaming states also activates dopamine signaling via the dopaminergic PDE neurons that appear to integrate the presence of food with the animal's own motion (Cermak et al, 2020). Activation of dopaminergic neurons during roaming elevates egg-laying rates, allowing animals disperse their eggs across bacterial food sources.…”

Doxycycline inhibits α-synuclein-associated pathologiesin vitroandin vivo

“…changes in cholinergic and GABAergic signaling due to D2 antagonism (Krum et al, 2020). Furthermore, it was also shown that changes in DA may affect GABAergic egg release in the worms (Cermak et al, 2020). These results demonstrate that further research into these pathways is necessary, but this is beyond the scope of our study.…”