Complex Locomotion Behavior Changes Are Induced in Caenorhabditis elegans by the Lack of the Regulatory Leak K+ Channel TWK-7

The change of locomotion activity in response to external cues is a considerable achievement of animals and is required for escape responses, foraging, and other complex behaviors. Little is known about the molecular regulators of such an adaptive locomotion. The conserved eukaryotic two-pore domain potassium (K2P) channels have been recognized as regulatory K+ channels that modify the membrane potential of cells, thereby affecting, e.g., rhythmic muscle activity. By using the Caenorhabditis elegans system combined with cell-type-specific approaches and locomotion in-depth analyses, here, we found that the loss of K2P channel TWK-7 increases the locomotor activity of worms during swimming and crawling in a coordinated mode. Moreover, loss of TWK-7 function results in a hyperactive state that (although less pronounced) resembles the fast, persistent, and directed forward locomotion behavior of stimulated C. elegans. TWK-7 is expressed in several head neurons as well as in cholinergic excitatory and GABAergic inhibitory motor neurons. Remarkably, the abundance of TWK-7 in excitatory B-type and inhibitory D-type motor neurons affected five central aspects of adaptive locomotion behavior: velocity/frequency, wavelength/amplitude, direction, duration, and straightness. Hence, we suggest that TWK-7 activity might represent a means to modulate a complex locomotion behavior at the level of certain types of motor neurons.