Antagonistic Inhibitory Circuits Integrate Visual and Gravitactic Behaviors

Larvae of the tunicate Ciona intestinalis possess a central nervous system of 177 neurons. This simplicity has facilitated the generation of a complete synaptic connectome. As chordates and the closest relatives of vertebrates, tunicates promise insight into the organization and evolution of vertebrate nervous systems. Ciona larvae have several sensory systems, including the ocellus and otolith, which are sensitive to light and gravity, respectively. Here, we describe circuitry by which these two are integrated into a complex behavior: the rapid reorientation of the body followed by upward swimming in response to dimming. Significantly, the gravity response causes an orienting behavior consisting of curved swims in downward-facing larvae but only when triggered by dimming. In contrast, the majority of larvae facing upward do not respond to dimming with orientation swims—but instead swim directly upward. Under constant light conditions, the gravity circuit appears to be inoperable, and both upward and downward swims were observed. Using connectomic and neurotransmitter data, we propose a circuit model that can account for these behaviors. The otolith consists of a statocyst cell and projecting excitatory sensory neurons (antenna cells). Postsynaptic to the antenna cells are a group of inhibitory primary interneurons, the antenna relay neurons (antRNs), which then project asymmetrically to the right and left motor units, thereby mediating curved orientation swims. Also projecting to the antRNs are inhibitory photoreceptor relay interneurons. These interneurons appear to antagonize the otolith circuit until they themselves are inhibited by photoreceptors in response to dimming, thus providing a triggering circuit. •Negative gravitaxis in Ciona larvae is triggered by dimming illumination•Inhibitory input from the visual system suppresses gravitaxis until dimming•Output from the gravitaxis organ results in asymmetric motor inhibition•Reorientation behavior is evoked in downward- but not upward-facing larvae Bostwick et al. investigate the neural circuity of gravitaxis in larvae of the simple chordate Ciona. The authors find that two inhibitory inputs, one that asymmetrically inhibits motor activity to elicit reorientation behavior and a second that serves to integrate visual cues with gravitaxis behavior, can account for observed behaviors.