Plasticity of paternity: Effects of fatherhood on synaptic, intrinsic and morphological characteristics of neurons in the medial preoptic area of male California mice

•California mouse fathers provide extensive paternal care to their offspring.•We compared properties of medial preoptic area neurons of fathers and virgin males.•Few differences were seen in intrinsic, synaptic, or morphological properties.•Synaptic inhibition was lower in fathers than in virgin mal...

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Veröffentlicht in:Behavioural brain research 2019-06, Vol.365, p.89-102
Hauptverfasser: Horrell, Nathan D., Saltzman, Wendy, Hickmott, Peter W.
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Saltzman, Wendy
Hickmott, Peter W.
description •California mouse fathers provide extensive paternal care to their offspring.•We compared properties of medial preoptic area neurons of fathers and virgin males.•Few differences were seen in intrinsic, synaptic, or morphological properties.•Synaptic inhibition was lower in fathers than in virgin males.•Fathers exhibited more paternal behavior toward unfamiliar pups than virgin males. Parental care by fathers enhances offspring survival and development in numerous species. In the biparental California mouse, Peromyscus californicus, behavioral plasticity is seen during the transition into fatherhood: adult virgin males often exhibit aggressive or indifferent responses to pups, whereas fathers engage in extensive paternal care. In this species and other biparental mammals, the onset of paternal behavior is associated with increased neural responsiveness to pups in specific brain regions, including the medial preoptic area of the hypothalamus (MPOA), a region strongly implicated in both maternal and paternal behavior. To assess possible changes in neural circuit properties underlying this increased excitability, we evaluated synaptic, intrinsic, and morphological properties of MPOA neurons in adult male California mice that were either virgins or first-time fathers. We used standard whole-cell recordings in a novel in vitro slice preparation. Excitatory and inhibitory post-synaptic currents from MPOA neurons were recorded in response to local electrical stimulation, and input/output curves were constructed for each. Responses to trains of stimuli were also examined. We quantified intrinsic excitability by measuring voltage changes in response to square-pulse injections of both depolarizing and hyperpolarizing current. Biocytin was injected into neurons during recording, and their morphology was analyzed. Most parameters did not differ significantly between virgins and fathers. However, we document a decrease in synaptic inhibition in fathers. These findings suggest that the onset of paternal behavior in California mouse fathers may be associated with limited electrophysiological plasticity within the MPOA.
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Parental care by fathers enhances offspring survival and development in numerous species. In the biparental California mouse, Peromyscus californicus, behavioral plasticity is seen during the transition into fatherhood: adult virgin males often exhibit aggressive or indifferent responses to pups, whereas fathers engage in extensive paternal care. In this species and other biparental mammals, the onset of paternal behavior is associated with increased neural responsiveness to pups in specific brain regions, including the medial preoptic area of the hypothalamus (MPOA), a region strongly implicated in both maternal and paternal behavior. To assess possible changes in neural circuit properties underlying this increased excitability, we evaluated synaptic, intrinsic, and morphological properties of MPOA neurons in adult male California mice that were either virgins or first-time fathers. We used standard whole-cell recordings in a novel in vitro slice preparation. Excitatory and inhibitory post-synaptic currents from MPOA neurons were recorded in response to local electrical stimulation, and input/output curves were constructed for each. Responses to trains of stimuli were also examined. We quantified intrinsic excitability by measuring voltage changes in response to square-pulse injections of both depolarizing and hyperpolarizing current. Biocytin was injected into neurons during recording, and their morphology was analyzed. Most parameters did not differ significantly between virgins and fathers. However, we document a decrease in synaptic inhibition in fathers. 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Parental care by fathers enhances offspring survival and development in numerous species. In the biparental California mouse, Peromyscus californicus, behavioral plasticity is seen during the transition into fatherhood: adult virgin males often exhibit aggressive or indifferent responses to pups, whereas fathers engage in extensive paternal care. In this species and other biparental mammals, the onset of paternal behavior is associated with increased neural responsiveness to pups in specific brain regions, including the medial preoptic area of the hypothalamus (MPOA), a region strongly implicated in both maternal and paternal behavior. To assess possible changes in neural circuit properties underlying this increased excitability, we evaluated synaptic, intrinsic, and morphological properties of MPOA neurons in adult male California mice that were either virgins or first-time fathers. We used standard whole-cell recordings in a novel in vitro slice preparation. Excitatory and inhibitory post-synaptic currents from MPOA neurons were recorded in response to local electrical stimulation, and input/output curves were constructed for each. Responses to trains of stimuli were also examined. We quantified intrinsic excitability by measuring voltage changes in response to square-pulse injections of both depolarizing and hyperpolarizing current. Biocytin was injected into neurons during recording, and their morphology was analyzed. Most parameters did not differ significantly between virgins and fathers. However, we document a decrease in synaptic inhibition in fathers. These findings suggest that the onset of paternal behavior in California mouse fathers may be associated with limited electrophysiological plasticity within the MPOA.</description><subject>Animals</subject><subject>Behavior, Animal - physiology</subject><subject>Brain - physiology</subject><subject>Electrophysiology</subject><subject>Fathers</subject><subject>Hypothalamus</subject><subject>Male</subject><subject>Medial preoptic area</subject><subject>Mice</subject><subject>Neuronal morphology</subject><subject>Neuronal Plasticity - physiology</subject><subject>Neurons - metabolism</subject><subject>Neurons - physiology</subject><subject>Parental behavior</subject><subject>Paternal Behavior - physiology</subject><subject>Peromyscus</subject><subject>Preoptic Area - metabolism</subject><subject>Preoptic Area - physiology</subject><issn>0166-4328</issn><issn>1872-7549</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kc2KFDEUhYMoTjv6AG4kSxdWm59KqqIgSDP-wIAudB3SqVtTaaqSMqke6BfyOb1lj4NuhEBIcs53b-4h5DlnW864fn3Y7vd5Kxg3WyZwmQdkw9tGVI2qzUOyQY2uainaC_KklANjrGaKPyYXkrVMKFlvyM-voytL8GE50dTT2S2QIx7e0Ku-B7-U9bZ3ywB5SKmjKdJyim5Gyysa4pJDLMFTFzs6pTwPaUw3wbuR-sFl55EWVvxvTIRjTrGgjSKPTtAFFM4Z0oqjLoNbZZMbge7cGPqErTg6BQ9PyaPejQWe3e2X5PuHq2-7T9X1l4-fd--vK18rvlSK-xaMaVqm-67X3AgtOtlJL5XS4HmttJIOoDZGi1rwvZFGQKNEzTsveSMvybszdz7usT8P-EM32jmHyeWTTS7Yf19iGOxNurVa60aqFfDyDpDTjyOUxU6heBhHFyEdixW81bzmWBKl_Cz1OZWSob8vw5ld87UHi_naNV_LBC6Dnhd_93fv-BMoCt6eBYBTug2QbfEBosdZZ4zTdin8B_8LD4G55Q</recordid><startdate>20190603</startdate><enddate>20190603</enddate><creator>Horrell, Nathan D.</creator><creator>Saltzman, Wendy</creator><creator>Hickmott, Peter W.</creator><general>Elsevier B.V</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20190603</creationdate><title>Plasticity of paternity: Effects of fatherhood on synaptic, intrinsic and morphological characteristics of neurons in the medial preoptic area of male California mice</title><author>Horrell, Nathan D. ; Saltzman, Wendy ; Hickmott, Peter W.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c451t-51c8e997806fdf619262d3d3c3556ec145653aee49962421b9392e75241dc3173</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Animals</topic><topic>Behavior, Animal - physiology</topic><topic>Brain - physiology</topic><topic>Electrophysiology</topic><topic>Fathers</topic><topic>Hypothalamus</topic><topic>Male</topic><topic>Medial preoptic area</topic><topic>Mice</topic><topic>Neuronal morphology</topic><topic>Neuronal Plasticity - physiology</topic><topic>Neurons - metabolism</topic><topic>Neurons - physiology</topic><topic>Parental behavior</topic><topic>Paternal Behavior - physiology</topic><topic>Peromyscus</topic><topic>Preoptic Area - metabolism</topic><topic>Preoptic Area - physiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Horrell, Nathan D.</creatorcontrib><creatorcontrib>Saltzman, Wendy</creatorcontrib><creatorcontrib>Hickmott, Peter W.</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Behavioural brain research</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Horrell, Nathan D.</au><au>Saltzman, Wendy</au><au>Hickmott, Peter W.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Plasticity of paternity: Effects of fatherhood on synaptic, intrinsic and morphological characteristics of neurons in the medial preoptic area of male California mice</atitle><jtitle>Behavioural brain research</jtitle><addtitle>Behav Brain Res</addtitle><date>2019-06-03</date><risdate>2019</risdate><volume>365</volume><spage>89</spage><epage>102</epage><pages>89-102</pages><issn>0166-4328</issn><eissn>1872-7549</eissn><abstract>•California mouse fathers provide extensive paternal care to their offspring.•We compared properties of medial preoptic area neurons of fathers and virgin males.•Few differences were seen in intrinsic, synaptic, or morphological properties.•Synaptic inhibition was lower in fathers than in virgin males.•Fathers exhibited more paternal behavior toward unfamiliar pups than virgin males. 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subjects Animals
Behavior, Animal - physiology
Brain - physiology
Electrophysiology
Fathers
Hypothalamus
Male
Medial preoptic area
Mice
Neuronal morphology
Neuronal Plasticity - physiology
Neurons - metabolism
Neurons - physiology
Parental behavior
Paternal Behavior - physiology
Peromyscus
Preoptic Area - metabolism
Preoptic Area - physiology
title Plasticity of paternity: Effects of fatherhood on synaptic, intrinsic and morphological characteristics of neurons in the medial preoptic area of male California mice
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