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Acute social isolation alters neurogenomic state in songbird forebrain.

ABSTRACT: Prolonged social isolation has negative effects on brain and behavior in humans and other social organisms, but neural mechanisms leading to these effects are not understood. Here we tested the hypothesis that even brief periods of social isolation can alter gene expression and DNA methylation in higher cognitive centers of the brain, focusing on the auditory/associative forebrain of the highly social zebra finch. Using RNA sequencing, we first identified genes that individually increase or decrease expression after isolation and observed general repression of gene sets annotated for neurotrophin pathways and axonal guidance functions. We then pursued 4 genes of large effect size: EGR1 and BDNF (decreased by isolation) and FKBP5 and UTS2B (increased). By in situ hybridization, each gene responded in different cell subsets, arguing against a single cellular mechanism. To test whether effects were specific to the social component of the isolation experience, we compared gene expression in birds isolated either alone or with a single familiar partner. Partner inclusion ameliorated the effect of solo isolation on EGR1 and BDNF, but not on FKBP5 and UTS2B nor on circulating corticosterone. By bisulfite sequencing analysis of auditory forebrain DNA, isolation caused changes in methylation of a subset of differentially expressed genes, including BDNF. Thus, social isolation has rapid consequences on gene activity in a higher integrative center of the brain, triggering epigenetic mechanisms that may influence processing of ongoing experience.

SUBMITTER: George JM

PROVIDER: S-EPMC7519284 | biostudies-literature | 2020 Sep

REPOSITORIES: biostudies-literature

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Acute social isolation alters neurogenomic state in songbird forebrain.

George Julia M JM Bell Zachary W ZW Condliffe Daniel D Dohrer Kirstin K Abaurrea Teresa T Spencer Karen K Leitão Albertine A Gahr Manfred M Hurd Paul J PJ Clayton David F DF

Proceedings of the National Academy of Sciences of the United States of America 20190722 38

Prolonged social isolation has negative effects on brain and behavior in humans and other social organisms, but neural mechanisms leading to these effects are not understood. Here we tested the hypothesis that even brief periods of social isolation can alter gene expression and DNA methylation in higher cognitive centers of the brain, focusing on the auditory/associative forebrain of the highly social zebra finch. Using RNA sequencing, we first identified genes that individually increase or decr ...[more]

PMID: 31332005

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Project description:Sensory responses to courtship signals can be altered by reproductive hormones. In seasonally-breeding female songbirds, for example, sound-induced immediate early gene expression in the auditory pathway is selective for male song over behaviourally irrelevant sounds only when plasma estradiol reaches breeding-like levels. This selectivity has been hypothesized to be mediated by release of monoaminergic neuromodulators in the auditory pathway. We previously showed that in oestrogen-primed female white-throated sparrows, exposure to male song induced dopamine and serotonin release in auditory regions. In order to mediate hormone-dependent selectivity, this release must be (1) selective for song and (2) modulated by endocrine state. Therefore, in the current study we addressed both questions by conducting playbacks of song or a control sound to females in a breeding-like or non-breeding endocrine state. We then used high performance liquid chromatography to measure turnover of dopamine, norepinephrine, and serotonin in the auditory midbrain and forebrain. We found that sound-induced turnover of dopamine and serotonin did in fact depend on endocrine state; hearing sound increased turnover in the auditory forebrain only in the birds in a breeding-like endocrine state. Contrary to our expectations, these increases occurred in response to either song or artificial tones; in other words, they were not selective for song. The selectivity of sound-induced monoamine release was thus strikingly different from that of immediate early gene responses described in previous studies. We did, however, find that constitutive monoamine release was altered by endocrine state; whether the birds heard sound or not, turnover of serotonin in the auditory forebrain was higher in a breeding-like state than in a non-breeding endocrine state. Our results suggest that dopaminergic and serotonergic responses to song and other sounds, as well as serotonergic tone in auditory areas, could be seasonally modulated. This article is protected by copyright. All rights reserved.

Dataset Information

Acute social isolation alters neurogenomic state in songbird forebrain.

Publications

Acute social isolation alters neurogenomic state in songbird forebrain.

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