The Serotonergic Control of Play Fighting in Male Juvenile Hamsters: Opposite Effects of 5‐HT 1A and 5‐HT 3 Receptor Manipulations

In male hamsters, puberty is associated with increased serotonin innervation and unusual responses to fluoxetine, such as enhanced play‐fighting activity against intruders but also an acceleration of its maturation from attacks focused on the face (frontal attacks) to the lower belly and rump, sugge...

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Published inDevelopmental psychobiology Vol. 67; no. 2; p. e70030
Main Authors Malone, Candice L., González‐Martínez, Lina Fernanda, Gray, Gabrielle E. J., Moran, Kevin M., Taravosh‐Lahn, Kereshmeh, Delville, Yvon
Format Journal Article
LanguageEnglish
Published United States 01.03.2025
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ISSN0012-1630
1098-2302
DOI10.1002/dev.70030

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Abstract In male hamsters, puberty is associated with increased serotonin innervation and unusual responses to fluoxetine, such as enhanced play‐fighting activity against intruders but also an acceleration of its maturation from attacks focused on the face (frontal attacks) to the lower belly and rump, suggesting a role for serotonin (5‐HT). We tested the role of 5‐HT 1A and 5‐HT 3 receptor subtypes on play‐fighting behavior observed during resident intruder tests through peripheral treatment with receptor agonists and antagonists. Contrary to observations in adult hamsters, we did not observe any overarching effects of treatment on measures of play‐fighting activity, nor its maturation from frontal attacks. However, secondary analyses highlighted variability within the datasets. A subgroup of animals presented inhibited play‐fighting activity in response to treatment with DPAT, a 5‐HT 1A receptor agonist, but these animals also showed enhanced locomotor activity and reduced interest in engaging their opponents. In addition, early juvenile agonistic behavior was predictive of responsiveness to other treatments. The 5‐HT 1A receptor antagonist, WAY, caused a reduction in play‐fighting activity in high attackers and an increase in low attackers. Though high attackers under pretest conditions were equally inhibited by CBG, a 5‐HT 3 receptor agonist, they performed a higher proportion of frontal attacks. Finally, the density of 5‐HT 1A and 5‐HT 3 receptor immunoreactivity was compared among subjects sampled at postnatal Day 35 (early puberty) or postnatal Day 70 (adulthood) within areas mediating the control of social behavior in adults. Adult males showed a higher density of immunolabeling for 5‐HT 1A receptors in the anterior hypothalamus and medial amygdala, as well as 5‐HT 3 receptors in the lateral septum. The data suggest that the development of 5‐HT receptor expression participates in the control of play‐fighting activity and its maturation during puberty in male hamsters.
AbstractList In male hamsters, puberty is associated with increased serotonin innervation and unusual responses to fluoxetine, such as enhanced play-fighting activity against intruders but also an acceleration of its maturation from attacks focused on the face (frontal attacks) to the lower belly and rump, suggesting a role for serotonin (5-HT). We tested the role of 5-HT and 5-HT receptor subtypes on play-fighting behavior observed during resident intruder tests through peripheral treatment with receptor agonists and antagonists. Contrary to observations in adult hamsters, we did not observe any overarching effects of treatment on measures of play-fighting activity, nor its maturation from frontal attacks. However, secondary analyses highlighted variability within the datasets. A subgroup of animals presented inhibited play-fighting activity in response to treatment with DPAT, a 5-HT receptor agonist, but these animals also showed enhanced locomotor activity and reduced interest in engaging their opponents. In addition, early juvenile agonistic behavior was predictive of responsiveness to other treatments. The 5-HT receptor antagonist, WAY, caused a reduction in play-fighting activity in high attackers and an increase in low attackers. Though high attackers under pretest conditions were equally inhibited by CBG, a 5-HT receptor agonist, they performed a higher proportion of frontal attacks. Finally, the density of 5-HT and 5-HT receptor immunoreactivity was compared among subjects sampled at postnatal Day 35 (early puberty) or postnatal Day 70 (adulthood) within areas mediating the control of social behavior in adults. Adult males showed a higher density of immunolabeling for 5-HT receptors in the anterior hypothalamus and medial amygdala, as well as 5-HT receptors in the lateral septum. The data suggest that the development of 5-HT receptor expression participates in the control of play-fighting activity and its maturation during puberty in male hamsters.
In male hamsters, puberty is associated with increased serotonin innervation and unusual responses to fluoxetine, such as enhanced play‐fighting activity against intruders but also an acceleration of its maturation from attacks focused on the face (frontal attacks) to the lower belly and rump, suggesting a role for serotonin (5‐HT). We tested the role of 5‐HT 1A and 5‐HT 3 receptor subtypes on play‐fighting behavior observed during resident intruder tests through peripheral treatment with receptor agonists and antagonists. Contrary to observations in adult hamsters, we did not observe any overarching effects of treatment on measures of play‐fighting activity, nor its maturation from frontal attacks. However, secondary analyses highlighted variability within the datasets. A subgroup of animals presented inhibited play‐fighting activity in response to treatment with DPAT, a 5‐HT 1A receptor agonist, but these animals also showed enhanced locomotor activity and reduced interest in engaging their opponents. In addition, early juvenile agonistic behavior was predictive of responsiveness to other treatments. The 5‐HT 1A receptor antagonist, WAY, caused a reduction in play‐fighting activity in high attackers and an increase in low attackers. Though high attackers under pretest conditions were equally inhibited by CBG, a 5‐HT 3 receptor agonist, they performed a higher proportion of frontal attacks. Finally, the density of 5‐HT 1A and 5‐HT 3 receptor immunoreactivity was compared among subjects sampled at postnatal Day 35 (early puberty) or postnatal Day 70 (adulthood) within areas mediating the control of social behavior in adults. Adult males showed a higher density of immunolabeling for 5‐HT 1A receptors in the anterior hypothalamus and medial amygdala, as well as 5‐HT 3 receptors in the lateral septum. The data suggest that the development of 5‐HT receptor expression participates in the control of play‐fighting activity and its maturation during puberty in male hamsters.
Author Malone, Candice L.
González‐Martínez, Lina Fernanda
Delville, Yvon
Moran, Kevin M.
Taravosh‐Lahn, Kereshmeh
Gray, Gabrielle E. J.
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  givenname: Lina Fernanda
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  fullname: González‐Martínez, Lina Fernanda
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  givenname: Gabrielle E. J.
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  fullname: Gray, Gabrielle E. J.
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  organization: Department of Psychology University of Texas at Austin Austin Texas USA
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Keywords juvenile hamsters
serotonin
5‐HT1A
5‐HT3
play fighting
agonistic behavior
puberty
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Snippet In male hamsters, puberty is associated with increased serotonin innervation and unusual responses to fluoxetine, such as enhanced play‐fighting activity...
In male hamsters, puberty is associated with increased serotonin innervation and unusual responses to fluoxetine, such as enhanced play-fighting activity...
SourceID pubmed
crossref
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StartPage e70030
SubjectTerms 8-Hydroxy-2-(di-n-propylamino)tetralin - pharmacology
Aggression - drug effects
Aggression - physiology
Animals
Behavior, Animal - drug effects
Behavior, Animal - physiology
Cricetinae
Male
Mesocricetus
Piperazines - pharmacology
Play and Playthings
Pyridines - pharmacology
Receptor, Serotonin, 5-HT1A - drug effects
Receptor, Serotonin, 5-HT1A - metabolism
Receptor, Serotonin, 5-HT1A - physiology
Receptors, Serotonin, 5-HT3 - drug effects
Receptors, Serotonin, 5-HT3 - metabolism
Receptors, Serotonin, 5-HT3 - physiology
Serotonin - metabolism
Serotonin 5-HT1 Receptor Agonists - pharmacology
Serotonin 5-HT3 Receptor Antagonists - pharmacology
Serotonin Receptor Agonists - pharmacology
Title The Serotonergic Control of Play Fighting in Male Juvenile Hamsters: Opposite Effects of 5‐HT 1A and 5‐HT 3 Receptor Manipulations
URI https://www.ncbi.nlm.nih.gov/pubmed/40007060
Volume 67
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