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Contributions of Luminance and Motion to Visual Escape and Habituation in Larval Zebrafish

Animals from insects to humans perform visual escape behavior in response to looming stimuli, and these responses habituate if looms are presented repeatedly without consequence. While the basic visual processing and motor pathways involved in this behavior have been described, many of the nuances o...

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Autores principales: Mancienne, Tessa, Marquez-Legorreta, Emmanuel, Wilde, Maya, Piber, Marielle, Favre-Bulle, Itia, Vanwalleghem, Gilles, Scott, Ethan K.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8568047/
https://www.ncbi.nlm.nih.gov/pubmed/34744637
http://dx.doi.org/10.3389/fncir.2021.748535
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author Mancienne, Tessa
Marquez-Legorreta, Emmanuel
Wilde, Maya
Piber, Marielle
Favre-Bulle, Itia
Vanwalleghem, Gilles
Scott, Ethan K.
author_facet Mancienne, Tessa
Marquez-Legorreta, Emmanuel
Wilde, Maya
Piber, Marielle
Favre-Bulle, Itia
Vanwalleghem, Gilles
Scott, Ethan K.
author_sort Mancienne, Tessa
collection PubMed
description Animals from insects to humans perform visual escape behavior in response to looming stimuli, and these responses habituate if looms are presented repeatedly without consequence. While the basic visual processing and motor pathways involved in this behavior have been described, many of the nuances of predator perception and sensorimotor gating have not. Here, we have performed both behavioral analyses and brain-wide cellular-resolution calcium imaging in larval zebrafish while presenting them with visual loom stimuli or stimuli that selectively deliver either the movement or the dimming properties of full loom stimuli. Behaviorally, we find that, while responses to repeated loom stimuli habituate, no such habituation occurs when repeated movement stimuli (in the absence of luminance changes) are presented. Dim stimuli seldom elicit escape responses, and therefore cannot habituate. Neither repeated movement stimuli nor repeated dimming stimuli habituate the responses to subsequent full loom stimuli, suggesting that full looms are required for habituation. Our calcium imaging reveals that motion-sensitive neurons are abundant in the brain, that dim-sensitive neurons are present but more rare, and that neurons responsive to both stimuli (and to full loom stimuli) are concentrated in the tectum. Neurons selective to full loom stimuli (but not to movement or dimming) were not evident. Finally, we explored whether movement- or dim-sensitive neurons have characteristic response profiles during habituation to full looms. Such functional links between baseline responsiveness and habituation rate could suggest a specific role in the brain-wide habituation network, but no such relationships were found in our data. Overall, our results suggest that, while both movement- and dim-sensitive neurons contribute to predator escape behavior, neither plays a specific role in brain-wide visual habituation networks or in behavioral habituation.
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spelling pubmed-85680472021-11-05 Contributions of Luminance and Motion to Visual Escape and Habituation in Larval Zebrafish Mancienne, Tessa Marquez-Legorreta, Emmanuel Wilde, Maya Piber, Marielle Favre-Bulle, Itia Vanwalleghem, Gilles Scott, Ethan K. Front Neural Circuits Neural Circuits Animals from insects to humans perform visual escape behavior in response to looming stimuli, and these responses habituate if looms are presented repeatedly without consequence. While the basic visual processing and motor pathways involved in this behavior have been described, many of the nuances of predator perception and sensorimotor gating have not. Here, we have performed both behavioral analyses and brain-wide cellular-resolution calcium imaging in larval zebrafish while presenting them with visual loom stimuli or stimuli that selectively deliver either the movement or the dimming properties of full loom stimuli. Behaviorally, we find that, while responses to repeated loom stimuli habituate, no such habituation occurs when repeated movement stimuli (in the absence of luminance changes) are presented. Dim stimuli seldom elicit escape responses, and therefore cannot habituate. Neither repeated movement stimuli nor repeated dimming stimuli habituate the responses to subsequent full loom stimuli, suggesting that full looms are required for habituation. Our calcium imaging reveals that motion-sensitive neurons are abundant in the brain, that dim-sensitive neurons are present but more rare, and that neurons responsive to both stimuli (and to full loom stimuli) are concentrated in the tectum. Neurons selective to full loom stimuli (but not to movement or dimming) were not evident. Finally, we explored whether movement- or dim-sensitive neurons have characteristic response profiles during habituation to full looms. Such functional links between baseline responsiveness and habituation rate could suggest a specific role in the brain-wide habituation network, but no such relationships were found in our data. Overall, our results suggest that, while both movement- and dim-sensitive neurons contribute to predator escape behavior, neither plays a specific role in brain-wide visual habituation networks or in behavioral habituation. Frontiers Media S.A. 2021-10-21 /pmc/articles/PMC8568047/ /pubmed/34744637 http://dx.doi.org/10.3389/fncir.2021.748535 Text en Copyright © 2021 Mancienne, Marquez-Legorreta, Wilde, Piber, Favre-Bulle, Vanwalleghem and Scott. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neural Circuits
Mancienne, Tessa
Marquez-Legorreta, Emmanuel
Wilde, Maya
Piber, Marielle
Favre-Bulle, Itia
Vanwalleghem, Gilles
Scott, Ethan K.
Contributions of Luminance and Motion to Visual Escape and Habituation in Larval Zebrafish
title Contributions of Luminance and Motion to Visual Escape and Habituation in Larval Zebrafish
title_full Contributions of Luminance and Motion to Visual Escape and Habituation in Larval Zebrafish
title_fullStr Contributions of Luminance and Motion to Visual Escape and Habituation in Larval Zebrafish
title_full_unstemmed Contributions of Luminance and Motion to Visual Escape and Habituation in Larval Zebrafish
title_short Contributions of Luminance and Motion to Visual Escape and Habituation in Larval Zebrafish
title_sort contributions of luminance and motion to visual escape and habituation in larval zebrafish
topic Neural Circuits
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8568047/
https://www.ncbi.nlm.nih.gov/pubmed/34744637
http://dx.doi.org/10.3389/fncir.2021.748535
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