Baier, H. | Search bioRxiv

bioRxiv2018

Biological motion as an innate perceptual mechanism driving social affiliation

Collective behavior, such as shoaling in teleost fish, is driven by the perceptual recognition of conspecific animals. Because social interactions are mutual, it has been difficult to disentangle the exact sensory cues that trigger affiliation in the first place from those that are emitted by receptive and responsive shoal mates. Here we overcome this challenge in a virtual reality assay in zebrafish. We discovered that simple visual features of conspecific biological motion provide an irresistible shoaling cue. Individual juvenile fish interact with circular black dots projected onto a screen, to the same extent as they do with real conspecifics, provided these virtual objects mimic the characteristic kinetics of zebrafish swim bouts. Other naturalistic cues previously implicated in shoaling, such as fish-like shape, pigmentation pattern, or non-visual sensory modalities are not required. During growth, the animals stimulus preferences shift gradually, matching self-like kinetics, even in fish raised in isolation. Virtual group interactions and our multi-agent model implementation of this perceptual mechanism demonstrate sufficiency of kinetic cues to drive assortative shoaling, a phenomenon commonly observed in field studies. Coordinated behavior can emerge from autonomous interactions, such as collective odor avoidance in Drosophila, or from reciprocal interactions, such as the codified turn-taking in wren duet singing. We found that individual zebrafish shoal autonomously without evidence for a reciprocal choreography. Our results reveal individual-level, innate perceptual rules of engagement in mutual affiliation and provide experimental access to the neural mechanisms of social recognition. (239/250 words max)\n\nSignificance StatementSocial affiliation is ubiquitous in the animal kingdom, but fundamental sensory cues driving group formation remain elusive. During swarm behavior, for example, individuals dynamically exchange sensory cues with their neighbors, presenting an intertwined choreography opaque to formal analysis of causal stimulus-response relationships. Using a virtual interaction assay for psychophysical analysis, we solved this issue and identify biological motion as the irresistible trigger of social affiliation in zebrafish, Danio rerio. Given that many species form groups including shoals, flocks and herds, perceptual mechanisms of social recognition and their underlying neural circuits are likely shared across vertebrates. The identification of fundamental affiliation-inducing cues is a prerequisite for relating individual-level sensory-motor transformations to collective behavior. (112/120 words max)

neuroscience↗

bioRxiv2017

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 neurites within the neuropil. Receptive field (RF) mapping revealed that SINs sample over large areas of the visual field (greater than 20 degrees, typically 50 degrees). 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.

neuroscience↗