Oxytocin Removes Estrous Female vs. Male Preference of Virgin Male Rats: Mediation of the Supraoptic Nucleus Via Olfactory Bulbs

Social functions of oxytocin (OT) have been explored extensively; however, relationship between the effect of intranasally applied OT (nasal OT) on the social preference (SP) and intracerebral actions of endogenous OT remains unclear. To resolve this question, we first observed effects of nasal OT o...

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Main Authors: Xiao-Yu Liu, Dan Cui, Dongyang Li, Runsheng Jiao, Xiaoran Wang, Shuwei Jia, Dan Hou, Tong Li, Haitao Liu, Ping Wang, Yu-Feng Wang
Format: Article
Language:English
Published: Frontiers Media S.A. 2017-10-01
Series:Frontiers in Cellular Neuroscience
Subjects:
Online Access:http://journal.frontiersin.org/article/10.3389/fncel.2017.00327/full
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author Xiao-Yu Liu
Dan Cui
Dongyang Li
Runsheng Jiao
Xiaoran Wang
Shuwei Jia
Dan Hou
Tong Li
Haitao Liu
Ping Wang
Yu-Feng Wang
author_facet Xiao-Yu Liu
Dan Cui
Dongyang Li
Runsheng Jiao
Xiaoran Wang
Shuwei Jia
Dan Hou
Tong Li
Haitao Liu
Ping Wang
Yu-Feng Wang
author_sort Xiao-Yu Liu
collection DOAJ
description Social functions of oxytocin (OT) have been explored extensively; however, relationship between the effect of intranasally applied OT (nasal OT) on the social preference (SP) and intracerebral actions of endogenous OT remains unclear. To resolve this question, we first observed effects of nasal OT on the SP of virgin young adult male rats toward unfamiliar virgin estrous female (EF) vs. virgin male rats. The results showed that the test male rats exhibited significantly more times and longer duration accessing the female than the male, which were acutely eliminated by nasal OT. Then, we examined the approaches mediating nasal OT effects on the activity of potential brain targets in Western blots and found that nasal OT activated the olfactory bulbs (OBs) and the supraoptic nucleus (SON), but not the piriform cortex, amygdala and hippocampus as shown by significant changes in the expression of c-Fos and/or phosphorylated extracellular signal-regulated protein kinase (pERK) 1/2. Moreover, microinjection of TTX into the OBs blocked nasal OT-evoked increases in pERK1/2 levels as well as the molecular association between ERK1/2 and OT-neurophysin in the SON. Electrolytic lesions of the lateral olfactory tract did not significantly change the basal levels of pERK 1/2 in the SON; however, upon nasal OT, pERK 1/2 levels in the SON reduced significantly. Lastly, microinjection of L-aminoadipic acid (gliotoxin) into the SON to reduce OT levels reduced the duration of the test male’s accessing the EF and blocked the nasal OT-evoked increase in the duration of test male’s accessing the male while significantly increasing pERK1/2 levels in the amygdala. These findings reveal for the first time that nasal OT acutely eliminates virgin males’ SP to EFs via the OB-SON route and that OT neurons could mediate the social effects of nasal OT by suppressing social phobia generated in the amygdala.
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spelling doaj.art-390783911e2c43b9810f096f5b7fa9c22022-12-22T02:05:07ZengFrontiers Media S.A.Frontiers in Cellular Neuroscience1662-51022017-10-011110.3389/fncel.2017.00327297431Oxytocin Removes Estrous Female vs. Male Preference of Virgin Male Rats: Mediation of the Supraoptic Nucleus Via Olfactory BulbsXiao-Yu Liu0Dan Cui1Dongyang Li2Runsheng Jiao3Xiaoran Wang4Shuwei Jia5Dan Hou6Tong Li7Haitao Liu8Ping Wang9Yu-Feng Wang10Department of Physiology, School of Basic Medical Sciences, Harbin Medical University, Harbin, ChinaDepartment of Physiology, School of Basic Medical Sciences, Harbin Medical University, Harbin, ChinaDepartment of Physiology, School of Basic Medical Sciences, Harbin Medical University, Harbin, ChinaDepartment of Physiology, School of Basic Medical Sciences, Harbin Medical University, Harbin, ChinaDepartment of Physiology, School of Basic Medical Sciences, Harbin Medical University, Harbin, ChinaDepartment of Physiology, School of Basic Medical Sciences, Harbin Medical University, Harbin, ChinaDepartment of Physiology, School of Basic Medical Sciences, Harbin Medical University, Harbin, ChinaDepartment of Physiology, School of Basic Medical Sciences, Harbin Medical University, Harbin, ChinaDepartment of Physiology, School of Basic Medical Sciences, Harbin Medical University, Harbin, ChinaDepartment of Genetics, School of Basic Medical Sciences, Harbin Medical University, Harbin, ChinaDepartment of Physiology, School of Basic Medical Sciences, Harbin Medical University, Harbin, ChinaSocial functions of oxytocin (OT) have been explored extensively; however, relationship between the effect of intranasally applied OT (nasal OT) on the social preference (SP) and intracerebral actions of endogenous OT remains unclear. To resolve this question, we first observed effects of nasal OT on the SP of virgin young adult male rats toward unfamiliar virgin estrous female (EF) vs. virgin male rats. The results showed that the test male rats exhibited significantly more times and longer duration accessing the female than the male, which were acutely eliminated by nasal OT. Then, we examined the approaches mediating nasal OT effects on the activity of potential brain targets in Western blots and found that nasal OT activated the olfactory bulbs (OBs) and the supraoptic nucleus (SON), but not the piriform cortex, amygdala and hippocampus as shown by significant changes in the expression of c-Fos and/or phosphorylated extracellular signal-regulated protein kinase (pERK) 1/2. Moreover, microinjection of TTX into the OBs blocked nasal OT-evoked increases in pERK1/2 levels as well as the molecular association between ERK1/2 and OT-neurophysin in the SON. Electrolytic lesions of the lateral olfactory tract did not significantly change the basal levels of pERK 1/2 in the SON; however, upon nasal OT, pERK 1/2 levels in the SON reduced significantly. Lastly, microinjection of L-aminoadipic acid (gliotoxin) into the SON to reduce OT levels reduced the duration of the test male’s accessing the EF and blocked the nasal OT-evoked increase in the duration of test male’s accessing the male while significantly increasing pERK1/2 levels in the amygdala. These findings reveal for the first time that nasal OT acutely eliminates virgin males’ SP to EFs via the OB-SON route and that OT neurons could mediate the social effects of nasal OT by suppressing social phobia generated in the amygdala.http://journal.frontiersin.org/article/10.3389/fncel.2017.00327/fullintranasal drug deliveryolfactory bulbsoxytocinsocial preferencesupraoptic nucleus
spellingShingle Xiao-Yu Liu
Dan Cui
Dongyang Li
Runsheng Jiao
Xiaoran Wang
Shuwei Jia
Dan Hou
Tong Li
Haitao Liu
Ping Wang
Yu-Feng Wang
Oxytocin Removes Estrous Female vs. Male Preference of Virgin Male Rats: Mediation of the Supraoptic Nucleus Via Olfactory Bulbs
Frontiers in Cellular Neuroscience
intranasal drug delivery
olfactory bulbs
oxytocin
social preference
supraoptic nucleus
title Oxytocin Removes Estrous Female vs. Male Preference of Virgin Male Rats: Mediation of the Supraoptic Nucleus Via Olfactory Bulbs
title_full Oxytocin Removes Estrous Female vs. Male Preference of Virgin Male Rats: Mediation of the Supraoptic Nucleus Via Olfactory Bulbs
title_fullStr Oxytocin Removes Estrous Female vs. Male Preference of Virgin Male Rats: Mediation of the Supraoptic Nucleus Via Olfactory Bulbs
title_full_unstemmed Oxytocin Removes Estrous Female vs. Male Preference of Virgin Male Rats: Mediation of the Supraoptic Nucleus Via Olfactory Bulbs
title_short Oxytocin Removes Estrous Female vs. Male Preference of Virgin Male Rats: Mediation of the Supraoptic Nucleus Via Olfactory Bulbs
title_sort oxytocin removes estrous female vs male preference of virgin male rats mediation of the supraoptic nucleus via olfactory bulbs
topic intranasal drug delivery
olfactory bulbs
oxytocin
social preference
supraoptic nucleus
url http://journal.frontiersin.org/article/10.3389/fncel.2017.00327/full
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