The superficial interneurons, SINs, of the zebrafish tectum, have been implicated in a range of visual functions, including size discrimination, directional selectivity, and looming‐evoked escape. This raises the question if SIN subpopulations, despite their morphological similarities and shared anatomical position in the retinotectal processing stream, carry out diverse, task‐specific functions in visual processing, or if they have simple tuning properties in common. Here we have further characterized the SINs through functional imaging, electrophysiological recordings, and neurotransmitter typing in two transgenic lines, the widely used Gal4s1156t and the recently reported LCRRH2‐RH2‐2:GFP. We found that about a third of the SINs strongly responded to changes in whole‐field light levels, with a strong preference for OFF over ON stimuli. Interestingly, individual SINs were selectively tuned to a diverse range of narrow luminance decrements. Overall responses to whole‐field luminance steps did not vary with the position of the SIN cell body along the depth of the tectal neuropil or with the orientation of its neurites. We ruled out the possibility that intrinsic photosensitivity of Gal4s1156t+ SINs contribute to the measured visual responses. We found that, while most SINs express GABAergic markers, a substantial minority express an excitatory neuronal marker, the vesicular glutamate transporter, expanding the possible roles of SIN function in the tectal circuitry. In conclusion, SINs represent a molecularly, morphologically, and functionally heterogeneous class of interneurons, with subpopulations that detect a range of specific visual features, to which we have now added narrow luminance decrements.

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 loomingevoked 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.

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