Zebrafish oxytocin neurons drive nocifensive behavior via brainstem premotor targets

Animals have evolved specialized neural circuits to defend themselves from pain- and injury-causing stimuli. Using a combination of optical, behavioral and genetic approaches in the larval zebrafish, we describe a novel role for hypothalamic oxytocin (OXT) neurons in the processing of noxious stimul...

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Published inNature neuroscience Vol. 22; no. 9; pp. 1477 - 1492
Main Authors Wee, Caroline L., Nikitchenko, Maxim, Wang, Wei-Chun, Luks-Morgan, Sasha J., Song, Erin, Gagnon, James A., Randlett, Owen, Bianco, Isaac H., Lacoste, Alix M. B., Glushenkova, Elena, Barrios, Joshua P., Schier, Alexander F., Kunes, Samuel, Engert, Florian, Douglass, Adam D.
Format Journal Article
LanguageEnglish
Published New York Nature Publishing Group US 01.09.2019
Nature Publishing Group
Subjects
14/35
14/63
14/69
631/378/2629
631/378/3920
64/116
Ablation
Activation
Animal behavior
Animal Genetics and Genomics
Animals
Behavior
Behavioral Sciences
Biological Techniques
Biomedical and Life Sciences
Biomedicine
Brain stem
Brain Stem - cytology
Brain Stem - physiology
Danio rerio
Defensive behavior
Genetic aspects
Hypothalamus
Hypothalamus - cytology
Hypothalamus - physiology
Neural networks
Neural Pathways - cytology
Neural Pathways - physiology
Neurobiology
Neurogenesis
Neurons
Neurosciences
Nociception - physiology
Nociceptors - cytology
Nociceptors - physiology
Oxytocin
Pain
Pain perception
Perceptual-motor processes
Physiological aspects
Receptors
Sensorimotor integration
Sensorimotor system
Sensory neurons
Stimuli
Zebra fish
Zebrafish
Online AccessGet full text
ISSN1097-6256
1546-1726
1546-1726
DOI10.1038/s41593-019-0452-x

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Abstract Animals have evolved specialized neural circuits to defend themselves from pain- and injury-causing stimuli. Using a combination of optical, behavioral and genetic approaches in the larval zebrafish, we describe a novel role for hypothalamic oxytocin (OXT) neurons in the processing of noxious stimuli. In vivo imaging revealed that a large and distributed fraction of zebrafish OXT neurons respond strongly to noxious inputs, including the activation of damage-sensing TRPA1 receptors. OXT population activity reflects the sensorimotor transformation of the noxious stimulus, with some neurons encoding sensory information and others correlating more strongly with large-angle swims. Notably, OXT neuron activation is sufficient to generate this defensive behavior via the recruitment of brainstem premotor targets, whereas ablation of OXT neurons or loss of the peptide attenuates behavioral responses to TRPA1 activation. These data highlight a crucial role for OXT neurons in the generation of appropriate defensive responses to noxious input. Detecting and responding to noxious stimuli is essential for survival. Wee et al. show that noxious stimuli elicit intense and widespread activity in zebrafish oxytocin neurons, which promote defensive behavior by activating hindbrain premotor neurons.
AbstractList Animals have evolved specialized neural circuits to defend themselves from pain- and injury-causing stimuli. Using a combination of optical, behavioral and genetic approaches in the larval zebrafish, we describe a novel role for hypothalamic oxytocin (OXT) neurons in the processing of noxious stimuli. In vivo imaging revealed that a large and distributed fraction of zebrafish OXT neurons respond strongly to noxious inputs, including the activation of damage-sensing TRPA1 receptors. OXT population activity reflects the sensorimotor transformation of the noxious stimulus, with some neurons encoding sensory information and others correlating more strongly with large-angle swims. Notably, OXT neuron activation is sufficient to generate this defensive behavior via the recruitment of brainstem premotor targets, whereas ablation of OXT neurons or loss of the peptide attenuates behavioral responses to TRPA1 activation. These data highlight a crucial role for OXT neurons in the generation of appropriate defensive responses to noxious input.
Animals have evolved specialized neural circuits to defend themselves from pain- and injury-causing stimuli. Using a combination of optical, behavioral and genetic approaches in the larval zebrafish, we describe a novel role for hypothalamic oxytocin (OXT) neurons in the processing of noxious stimuli. In vivo imaging revealed that a large and distributed fraction of zebrafish OXT neurons respond strongly to noxious inputs, including the activation of damage-sensing TRPA1 receptors. OXT population activity reflects the sensorimotor transformation of the noxious stimulus, with some neurons encoding sensory information and others correlating more strongly with large-angle swims. Notably, OXT neuron activation is sufficient to generate this defensive behavior via the recruitment of brainstem premotor targets, whereas ablation of OXT neurons or loss of the peptide attenuates behavioral responses to TRPA1 activation. These data highlight a crucial role for OXT neurons in the generation of appropriate defensive responses to noxious input. Detecting and responding to noxious stimuli is essential for survival. Wee et al. show that noxious stimuli elicit intense and widespread activity in zebrafish oxytocin neurons, which promote defensive behavior by activating hindbrain premotor neurons.
Animals have evolved specialized neural circuits to defend themselves from pain- and injury-causing stimuli. Using a combination of optical, behavioral and genetic approaches in the larval zebrafish, we describe a novel role for hypothalamic oxytocin (OXT) neurons in the processing of noxious stimuli. In vivo imaging revealed that a large and distributed fraction of zebrafish OXT neurons respond strongly to noxious inputs, including the activation of damage-sensing TRPA1 receptors. OXT population activity reflects the sensorimotor transformation of the noxious stimulus, with some neurons encoding sensory information and others correlating more strongly with large-angle swims. Notably, OXT neuron activation is sufficient to generate this defensive behavior via the recruitment of brainstem premotor targets, whereas ablation of OXT neurons or loss of the peptide attenuates behavioral responses to TRPA1 activation. These data highlight a crucial role for OXT neurons in the generation of appropriate defensive responses to noxious input.Animals have evolved specialized neural circuits to defend themselves from pain- and injury-causing stimuli. Using a combination of optical, behavioral and genetic approaches in the larval zebrafish, we describe a novel role for hypothalamic oxytocin (OXT) neurons in the processing of noxious stimuli. In vivo imaging revealed that a large and distributed fraction of zebrafish OXT neurons respond strongly to noxious inputs, including the activation of damage-sensing TRPA1 receptors. OXT population activity reflects the sensorimotor transformation of the noxious stimulus, with some neurons encoding sensory information and others correlating more strongly with large-angle swims. Notably, OXT neuron activation is sufficient to generate this defensive behavior via the recruitment of brainstem premotor targets, whereas ablation of OXT neurons or loss of the peptide attenuates behavioral responses to TRPA1 activation. These data highlight a crucial role for OXT neurons in the generation of appropriate defensive responses to noxious input.
Animals have evolved specialized neural circuits to defend themselves from pain- and injury-causing stimuli. Using a combination of optical, behavioral and genetic approaches in the larval zebrafish, we describe a novel role for hypothalamic oxytocin (OXT) neurons in the processing of noxious stimuli. In vivo imaging revealed that a large and distributed fraction of zebrafish OXT neurons respond strongly to noxious inputs, including the activation of damage-sensing TRPA1 receptors. OXT population activity reflects the sensorimotor transformation of the noxious stimulus, with some neurons encoding sensory information and others correlating more strongly with large-angle swims. Notably, OXT neuron activation is sufficient to generate this defensive behavior via the recruitment of brainstem premotor targets, whereas ablation of OXT neurons or loss of the peptide attenuates behavioral responses to TRPA1 activation. These data highlight a crucial role for OXT neurons in the generation of appropriate defensive responses to noxious input. Detecting and responding to noxious stimuli is essential for survival. Wee et al. show that noxious stimuli elicit intense and widespread activity in zebrafish oxytocin neurons, which promote defensive behavior by activating hindbrain premotor neurons.
Animals have evolved specialized neural circuits to defend themselves from pain- and injury-causing stimuli. Using a combination of optical, behavioral and genetic approaches in the larval zebrafish, we describe a novel role for hypothalamic oxytocin (OXT) neurons in the processing of noxious stimuli. In vivo imaging reveals that a large and distributed fraction of zebrafish OXT neurons responds strongly to noxious inputs, including the activation of damage-sensing TRPA1 receptors. OXT population activity reflects the sensorimotor transformation of the noxious stimulus, with some neurons encoding sensory information and others correlating more strongly with large-angle swims. Notably, OXT neuron activation is sufficient to generate this defensive behavior via the recruitment of brainstem premotor targets, whereas ablation of OXT neurons or loss of the peptide attenuate behavioral responses to TRPA1 activation. These data highlight a crucial role for OXT neurons in the generation of appropriate defensive responses to noxious input.
Audience Academic
Author Song, Erin
Luks-Morgan, Sasha J.
Engert, Florian
Bianco, Isaac H.
Douglass, Adam D.
Wang, Wei-Chun
Gagnon, James A.
Randlett, Owen
Schier, Alexander F.
Nikitchenko, Maxim
Glushenkova, Elena
Kunes, Samuel
Barrios, Joshua P.
Lacoste, Alix M. B.
Wee, Caroline L.
AuthorAffiliation 1 Department of Molecular and Cellular Biology and Center for Brain Science, Harvard University, Cambridge, Massachusetts, USA
4 Center for Brain Science, Harvard University, Cambridge, Massachusetts, USA
2 Program in Neuroscience, Department of Neurobiology, Harvard Medical School, Boston, Massachusetts, USA
5 Broad Institute of MIT and Harvard, Cambridge, Massachusetts, USA
6 Harvard Stem Cell Institute, Cambridge, Massachusetts, USA
8 Present address: Department of Biology, University of Utah, Salt Lake City, Utah, USA
9 Present address: Department of Neuroscience, Physiology & Pharmacology, University College London, London, UK
3 Department of Neurobiology and Anatomy, University of Utah, Salt Lake City, Utah, USA
7 FAS Center for Systems Biology, Harvard University, Massachusetts, USA
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/31358991$$D View this record in MEDLINE/PubMed
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AUTHOR CONTRIBUTIONS
C.L.W., A.D.D. & F.E. conceived of the project, with critical advice and guidance from S.K., E.S. and M.N. A.D.D. & F.E. supervised the project. C.L.W. designed and performed most of the experiments, and analyzed most of the data. M.N. developed hardware and software for calcium imaging and behavioral experiments, designed and performed some experiments and analyzed the free-swimming behavioral data. W.C.W. & S.L.-M. performed experiments and analyzed data; E.S., O.R., A.M.B.L. & E.G. performed experiments; J.P.B. developed software for behavioral analysis. I.H.B. developed the optogenetic stimulation setup and advised experiments. J.G. and C.L.W. generated the oxytocin CRISPR mutant. A.D.D. and C.L.W. generated the Tg(oxt:Gal4) line. A.F.S. supervised J.G., O.R. & A.M.B.L. and advised the project. C.L.W. and A.D.D. wrote the manuscript with contribution from all other authors.
ORCID 0000-0001-7859-314X
0000-0003-1618-6244
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0000-0002-9353-6706
0000-0001-8169-2990
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Snippet Animals have evolved specialized neural circuits to defend themselves from pain- and injury-causing stimuli. Using a combination of optical, behavioral and...
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StartPage 1477
SubjectTerms 14/35
14/63
14/69
631/378/2629
631/378/3920
64/116
Ablation
Activation
Animal behavior
Animal Genetics and Genomics
Animals
Behavior
Behavioral Sciences
Biological Techniques
Biomedical and Life Sciences
Biomedicine
Brain stem
Brain Stem - cytology
Brain Stem - physiology
Danio rerio
Defensive behavior
Genetic aspects
Hypothalamus
Hypothalamus - cytology
Hypothalamus - physiology
Neural networks
Neural Pathways - cytology
Neural Pathways - physiology
Neurobiology
Neurogenesis
Neurons
Neurosciences
Nociception - physiology
Nociceptors - cytology
Nociceptors - physiology
Oxytocin
Pain
Pain perception
Perceptual-motor processes
Physiological aspects
Receptors
Sensorimotor integration
Sensorimotor system
Sensory neurons
Stimuli
Zebra fish
Zebrafish
Title Zebrafish oxytocin neurons drive nocifensive behavior via brainstem premotor targets
URI https://link.springer.com/article/10.1038/s41593-019-0452-x
https://www.ncbi.nlm.nih.gov/pubmed/31358991
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https://www.proquest.com/docview/2267026115
https://pubmed.ncbi.nlm.nih.gov/PMC6820349
Volume 22
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