Detection of whole-field luminance changes by superficial interneurons in the zebrafish tectum

The superficial interneurons, SINs, of the zebrafish tectum, also known as tectal horizontal cells, have been implicated in a range of behavioral responses to visual cues, including prey capture and looming-evoked escape. However, there is limited information on their tuning properties, synaptic connectivity and molecular diversity. We have begun to close this gap in our knowledge by performing functional GCaMP6 imaging and electrophysiological recordings of SIN responses to simplified stimuli. We found that a large subset of the SINs strongly responded to luminance changes, with a preference for OFF steps. Although SINs were generally tuned to any dark-light, or light-dark, transition, they were often most sensitive to a narrow range of luminance steps. Tuning properties did not vary with the position of the SIN cell body along the depth of the tectal neuropil or with the orientation of the cell’s neurites within the neuropil. Receptive field (RF) mapping revealed that SINs sample over large areas of the visual field (>20°, typically 50°). RFs of individual SINs were sometimes spatially incoherent, indicating that SINs may receive sparse inputs from multiple RGCs scattered widely over the retina. Lastly, we found that, while most SINs express GABAergic markers, as reported before, a substantial minority express a vesicular glutamate transporter. We propose that the role of the SINs is more complex than previously reported, and provide evidence that at least one SIN subtype could function as a multi-purpose circuit element for signaling changes in ambient luminance for subsequent processing in the tectum.