Peripheral oxytocin injection modulates vomeronasal sensory activity and reduces pup-directed aggression in male mice

Behaviors are shaped by hormones, which may act either by changing brain circuits or by modifying sensory detection of relevant cues. Pup-directed behaviors have been previously shown to change via action of hormones at the brain level. Here, we investigated hormonal control of pup-induced activity...

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Published inScientific reports Vol. 10; no. 1; p. 19943
Main Authors Nakahara, Thiago S., Camargo, Antonio P., Magalhães, Pedro H. M., Souza, Mateus A. A., Ribeiro, Pedro G., Martins-Netto, Paulo H., Carvalho, Vinicius M. A., José, Juliana, Papes, Fabio
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 17.11.2020
Nature Publishing Group
Subjects
631/378/2624
631/378/3917
631/378/3919
Aggression - drug effects
Aggression - physiology
Aggressive behavior
Animals
Animals, Newborn
Behavior
Biomarkers - analysis
Chemoreception
Female
Females
G protein-coupled receptors
Hormones
Humanities and Social Sciences
Hybridization
Injection
Male
Mice
multidisciplinary
Olfactory pathways
Oxytocics - administration & dosage
Oxytocics - pharmacology
Oxytocin
Oxytocin - administration & dosage
Oxytocin - pharmacology
Receptors, Oxytocin - metabolism
Ribonucleic acid
RNA
RNA-Seq
Science
Science (multidisciplinary)
Sensory epithelium
Social behavior
Vasopressin
Vasopressin receptors
Vomeronasal organ
Vomeronasal Organ - drug effects
Vomeronasal Organ - physiology
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Abstract Behaviors are shaped by hormones, which may act either by changing brain circuits or by modifying sensory detection of relevant cues. Pup-directed behaviors have been previously shown to change via action of hormones at the brain level. Here, we investigated hormonal control of pup-induced activity in the vomeronasal organ, an olfactory sensory structure involved in the detection of non-volatile chemosignals. Vomeronasal activity decreases as males switch from a pup-aggressive state to a non-aggressive parenting state, after they socially contact a female. RNA sequencing, qPCR, and in situ hybridization were used to identify expression, in the vomeronasal sensory epithelium, of candidate GPCR hormone receptors chosen by in silico analyses and educated guesses. After identifying that oxytocin and vasopressin receptors are expressed in the vomeronasal organ, we injected the corresponding hormones in mice and showed that oxytocin administration reduced both pup-induced vomeronasal activity and aggressive behavior. Conversely, injection of an oxytocin receptor antagonist in female-primed male animals, which normally exhibit reduced vomeronasal activity, significantly increased the number of active vomeronasal neurons. These data link oxytocin to the modulation of olfactory sensory activity, providing a possible mechanism for changes in male behavior after social experience with females.
AbstractList Behaviors are shaped by hormones, which may act either by changing brain circuits or by modifying sensory detection of relevant cues. Pup-directed behaviors have been previously shown to change via action of hormones at the brain level. Here, we investigated hormonal control of pup-induced activity in the vomeronasal organ, an olfactory sensory structure involved in the detection of non-volatile chemosignals. Vomeronasal activity decreases as males switch from a pup-aggressive state to a non-aggressive parenting state, after they socially contact a female. RNA sequencing, qPCR, and in situ hybridization were used to identify expression, in the vomeronasal sensory epithelium, of candidate GPCR hormone receptors chosen by in silico analyses and educated guesses. After identifying that oxytocin and vasopressin receptors are expressed in the vomeronasal organ, we injected the corresponding hormones in mice and showed that oxytocin administration reduced both pup-induced vomeronasal activity and aggressive behavior. Conversely, injection of an oxytocin receptor antagonist in female-primed male animals, which normally exhibit reduced vomeronasal activity, significantly increased the number of active vomeronasal neurons. These data link oxytocin to the modulation of olfactory sensory activity, providing a possible mechanism for changes in male behavior after social experience with females.
Behaviors are shaped by hormones, which may act either by changing brain circuits or by modifying sensory detection of relevant cues. Pup-directed behaviors have been previously shown to change via action of hormones at the brain level. Here, we investigated hormonal control of pup-induced activity in the vomeronasal organ, an olfactory sensory structure involved in the detection of non-volatile chemosignals. Vomeronasal activity decreases as males switch from a pup-aggressive state to a non-aggressive parenting state, after they socially contact a female. RNA sequencing, qPCR, and in situ hybridization were used to identify expression, in the vomeronasal sensory epithelium, of candidate GPCR hormone receptors chosen by in silico analyses and educated guesses. After identifying that oxytocin and vasopressin receptors are expressed in the vomeronasal organ, we injected the corresponding hormones in mice and showed that oxytocin administration reduced both pup-induced vomeronasal activity and aggressive behavior. Conversely, injection of an oxytocin receptor antagonist in female-primed male animals, which normally exhibit reduced vomeronasal activity, significantly increased the number of active vomeronasal neurons. These data link oxytocin to the modulation of olfactory sensory activity, providing a possible mechanism for changes in male behavior after social experience with females.Behaviors are shaped by hormones, which may act either by changing brain circuits or by modifying sensory detection of relevant cues. Pup-directed behaviors have been previously shown to change via action of hormones at the brain level. Here, we investigated hormonal control of pup-induced activity in the vomeronasal organ, an olfactory sensory structure involved in the detection of non-volatile chemosignals. Vomeronasal activity decreases as males switch from a pup-aggressive state to a non-aggressive parenting state, after they socially contact a female. RNA sequencing, qPCR, and in situ hybridization were used to identify expression, in the vomeronasal sensory epithelium, of candidate GPCR hormone receptors chosen by in silico analyses and educated guesses. After identifying that oxytocin and vasopressin receptors are expressed in the vomeronasal organ, we injected the corresponding hormones in mice and showed that oxytocin administration reduced both pup-induced vomeronasal activity and aggressive behavior. Conversely, injection of an oxytocin receptor antagonist in female-primed male animals, which normally exhibit reduced vomeronasal activity, significantly increased the number of active vomeronasal neurons. These data link oxytocin to the modulation of olfactory sensory activity, providing a possible mechanism for changes in male behavior after social experience with females.
ArticleNumber 19943
Author Magalhães, Pedro H. M.
Martins-Netto, Paulo H.
Papes, Fabio
Ribeiro, Pedro G.
José, Juliana
Souza, Mateus A. A.
Nakahara, Thiago S.
Carvalho, Vinicius M. A.
Camargo, Antonio P.
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  givenname: Antonio P.
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  givenname: Pedro H. M.
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  givenname: Pedro G.
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  givenname: Vinicius M. A.
  surname: Carvalho
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  email: papesf@unicamp.br
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/33203885$$D View this record in MEDLINE/PubMed
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Snippet Behaviors are shaped by hormones, which may act either by changing brain circuits or by modifying sensory detection of relevant cues. Pup-directed behaviors...
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SubjectTerms 631/378/2624
631/378/3917
631/378/3919
Aggression - drug effects
Aggression - physiology
Aggressive behavior
Animals
Animals, Newborn
Behavior
Biomarkers - analysis
Chemoreception
Female
Females
G protein-coupled receptors
Hormones
Humanities and Social Sciences
Hybridization
Injection
Male
Mice
multidisciplinary
Olfactory pathways
Oxytocics - administration & dosage
Oxytocics - pharmacology
Oxytocin
Oxytocin - administration & dosage
Oxytocin - pharmacology
Receptors, Oxytocin - metabolism
Ribonucleic acid
RNA
RNA-Seq
Science
Science (multidisciplinary)
Sensory epithelium
Social behavior
Vasopressin
Vasopressin receptors
Vomeronasal organ
Vomeronasal Organ - drug effects
Vomeronasal Organ - physiology
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Title Peripheral oxytocin injection modulates vomeronasal sensory activity and reduces pup-directed aggression in male mice
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