The tunicateCionais the only chordate with a fully-described connectome. Minimal circuits underlying a number of larval behaviors have been described, including for negative phototaxis. InCionalarvae, negative phototaxis initiates via rhythmic spontaneous casting swims. As the larvae cast in a light field, their photoreceptors will be directionally shaded with the aid of a pigment cell, providing a phototactic cue. We report here that the larval forebrain ofCionahas a previously uncharacterized single slow-oscillating inhibitory neuron (neuron BVIN78) that projects to the midbrain, where it targets key interneurons of the phototaxis circuit known as thephotoreceptor relay neurons. The anatomical location, gene expression and oscillation of BVIN78 indicate homology to oscillating neurons of the vertebrate hypothalamus. Ablation of BVIN78 results in larvae showing spontaneous swims that mimic phototaxis, but which occur in the absence of phototactic cues. Thus, BVIN78 has a gating activity on phototaxis by projecting temporally oscillating inhibition to the circuit. The frequency of BVIN78 oscillation does not match that of the rhythmic spontaneous swims, indicating that it does not initiate swims, but rather modulates them temporally. We speculate that its function is to add noise to what would otherwise be predictable behavior.