Characterization of a thalamic nucleus mediating habenula responses to changes in ambient illumination

Ruey-Kuang Cheng, Seetha Krishnan, Qian Lin, Caroline Kibat, Suresh Jesuthasan

Neural activity in the vertebrate habenula is affected by ambient illumination. The nucleus that links photoreceptor activity with the habenula is not well characterized. Here, we describe the location, inputs and potential function of this nucleus in larval zebrafish. High-speed calcium imaging shows that light ON and OFF both evoke a rapid response in the dorsal left neuropil of the habenula, indicating preferential targeting of this neuropil by afferents conveying information about ambient illumination. Injection of a lipophilic dye into this neuropil led to bilateral labeling of a nucleus in the anterior thalamus that responds to light ON and OFF, and that receives innervation from the retina and pineal organ. Lesioning the neuropil of this thalamic nucleus reduced the habenula response to light ON and OFF. Optogenetic stimulation of the thalamus with channelrhodopsin-2 caused depolarization in the habenula, while manipulation with anion channelrhodopsins inhibited habenula response to light and disrupted climbing and diving evoked by illumination change. A nucleus in the anterior thalamus of larval zebrafish innervates the dorsal left habenula. This nucleus receives input from the retina and pineal, responds to increase and decrease in ambient illumination, enables habenula responses to change in irradiance, and may function in light-evoked vertical migration.