Neural circuits underlying habituation of visually evoked escape behaviors in larval zebrafish
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eLife assessment
In the present study, the authors discovered the inhibitory neurons that are potentiated during the repetitive visual stimuli and control neurons that transmit looming information to evoke escape responses. Thus, the study elucidated a principle of habituation using a model vertebrate zebrafish.
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Abstract
Larval zebrafish that are exposed repeatedly to dark looming stimuli will quickly habituate to these aversive signals and cease to respond with their stereotypical escape swims. A dark looming stimulus can be separated into two independent components: one that is characterized by an overall spatial expansion, where overall luminance is maintained at the same level, and a second, that represents an overall dimming within the whole visual field in the absence of any motion energy. Using specific stimulation patterns that isolate these independent components, we first extracted the behavioral algorithms that dictate how these separate information channels interact with each other and across the two eyes during the habituation process. Concurrent brain wide imaging experiments then permitted the construction of circuit models that suggest the existence of two separate neural pathways. The first is a looming channel which responds specifically to expanding edges presented to the contralateral eye and relays that information to the brain stem escape network to generate directed escapes. The second is a dimming-specific channel that could be either monocular or binocularly responsive, and that appears to specifically inhibit escape response when activated. We propose that this second channel is under strong contextual modulation and that it is primarily responsible for the incremental silencing of successive dark looming-evoked escapes.
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eLife assessment
In the present study, the authors discovered the inhibitory neurons that are potentiated during the repetitive visual stimuli and control neurons that transmit looming information to evoke escape responses. Thus, the study elucidated a principle of habituation using a model vertebrate zebrafish.
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Reviewer #1 (Public Review):
In the present manuscript, the authors investigated circuits mechanisms that underlie habituation of visually evoked escape behaviors in larval zebrafish. For eliciting escape behaviors, the authors used dark looming stimuli. Larvae habituate to repeated stimulation with dark looming stimuli. The authors decomposed a dark looming stimulus into two independent components: one that is characterized by an overall spatial expansion, and the other that represents an overall dimming within the whole visual field. The authors found that pre-exposure to just the dimming component habituates responsiveness to dark looming in a comparable fashion than repeated exposure to the full dark looming. They investigated neural mechanisms that account for this using two photon calcium imaging experiments. Based on the results, …
Reviewer #1 (Public Review):
In the present manuscript, the authors investigated circuits mechanisms that underlie habituation of visually evoked escape behaviors in larval zebrafish. For eliciting escape behaviors, the authors used dark looming stimuli. Larvae habituate to repeated stimulation with dark looming stimuli. The authors decomposed a dark looming stimulus into two independent components: one that is characterized by an overall spatial expansion, and the other that represents an overall dimming within the whole visual field. The authors found that pre-exposure to just the dimming component habituates responsiveness to dark looming in a comparable fashion than repeated exposure to the full dark looming. They investigated neural mechanisms that account for this using two photon calcium imaging experiments. Based on the results, the authors propose a circuits model where a subset of inhibitory DS (dimming sensitive) neurons are incrementally potentiated by repetitive stimulation and where these neurons serve to locally depress the looming selective relay pathway.
There are two caveats in the present study. First, there exists another independent habituation pathway as habituation also occurs for spatial expansion stimuli that do not accompany dimming (checkerboard stimuli). This manuscript does not investigate neural mechanisms of this habituation pathway at all. Second, the authors performed no experiment that supports the validity of the model (i.e., no ablation experiment). These two caveats reduce the impact of the manuscript. Nevertheless, I think the manuscript is worth publishing, as the model the authors propose is interesting. The model generates a series of predictions about behavior, neural response properties and synaptic connectivity, which, I hope, will be tested in future experiments.
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Reviewer #2 (Public Review):
Overall, the greatest value of this article lies in the discovery and statistics of the inhibitory components that increased in response to continuous repetitive visual stimuli and suppressed responses of the critical neurons that transmit looming information to elicit escape. Although the author proposes a possible mechanism for visual habituation in larva zebrafish, there are still some shortcomings in the circuitry level proof and data interpretation, most conclusions in Figures 1-5 have been drawn in other work and lack certain innovations. In general, the overall logic of this article is relatively complete and the content is substantial, many data are very interesting and worth further interpretation.
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