Juvenile stress exerts sex-independent effects on anxiety, antidepressant-like behaviours and dopaminergic innervation of the prelimbic cortex in adulthood and does not alter hippocampal neurogenesis

Harris, Erin P.; McGovern, Andrew J.; Melo, Thieza G.; Barron, Aaron; Nola, Yvonne M.; O’Leary, Olivia F.

doi:10.1016/j.bbr.2021.113725

Cited by 7 publications

(5 citation statements)

References 106 publications

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“…Additionally, 3 weeks of post-weaning social isolation had no effect on anxiety-like behaviors in female rats [ 10 ]. Moreover, our results are echoed by previous studies showing that social isolation in adolescence from PD30 to PD50 had no effect on depression-like behavior in female rats [ 44 , 45 ]. Thus, it is important to note that because of differences in separation length, behavioral testing timing and experimental design, social-isolation stress may have inconsistent behavioral results [ 4 ].…”

Section: Discussionsupporting

confidence: 78%

Protective Effects of Resveratrol on Adolescent Social Isolation-Induced Anxiety-Like Behaviors via Modulating Nucleus Accumbens Spine Plasticity and Mitochondrial Function in Female Rats

Zhao

Liu

et al. 2022

Nutrients

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Social isolation (SI) is a major risk factor for mood disorders in adolescents. The nucleus accumbens (NAc) is an important reward center implicated in psychiatric disorders. Resveratrol (RSV) is one of the most effective natural polyphenols with anti-anxiety and depression effects. However, little is known about the therapeutic effects and mechanisms of RSV on behavioral abnormality of adolescent social stress. Therefore, this study aimed to investigate the underlying mechanism of RSV on the amelioration of SI-induced behavioral abnormality. We found that SI induced anxiety-like behavior and social dysfunction in isolated female rats. Moreover, SI reduced mitochondrial number and ATP levels and increased thin spine density in the NAc. RNA sequencing results showed that SI changed the transcription pattern in the NAc, including 519 upregulated genes and 610 downregulated genes, especially those related to mitochondrial function. Importantly, RSV ameliorated behavioral and spine abnormalities induced by SI and increased NAc ATP levels and mitochondria number. Furthermore, RSV increased the activity of cytochrome C oxidase (COX) and upregulated mRNA levels of Cox5a, Cox6a1 and Cox7c. These results demonstrate that the modulation of spine plasticity and mitochondrial function in the NAc by RSV has a therapeutic effect on mood disorders induced by social isolation.

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Section: Discussionsupporting

confidence: 78%

Protective Effects of Resveratrol on Adolescent Social Isolation-Induced Anxiety-Like Behaviors via Modulating Nucleus Accumbens Spine Plasticity and Mitochondrial Function in Female Rats

Zhao

Liu

et al. 2022

Nutrients

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“…This suggests that stressor timing during adolescence can influence the direction of dopamine alterations. Supporting this, immunostaining for tyrosine hydroxylase increased in layer I of the PL cortex of male and female rats stressed from PND 27–29, a relatively short period of time immediately surrounding the start of adolescence ( Harris et al, 2022 ). Exposure to a predator odor during adolescence reduced D2R expression in the medial PFC in adulthood ( Wright et al, 2008 ), perhaps indicating compensation for changes in dopamine levels following adolescent stress.…”

Section: Animal Studies Of Adolescent Stressmentioning

confidence: 74%

Adolescent Alcohol and Stress Exposure Rewires Key Cortical Neurocircuitry

et al. 2022

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Human adolescence is a period of development characterized by wide ranging emotions and behavioral risk taking, including binge drinking (Konrad et al., 2013). These behavioral manifestations of adolescence are complemented by growth in the neuroarchitecture of the brain, including synaptic pruning (Spear, 2013) and increases in overall white matter volume (Perrin et al., 2008). During this period of profound physiological maturation, the adolescent brain has a unique vulnerability to negative perturbations. Alcohol consumption and stress exposure, both of which are heightened during adolescence, can individually and synergistically alter these neurodevelopmental trajectories in positive and negative ways (conferring both resiliency and susceptibility) and influence already changing neurotransmitter systems and circuits. Importantly, the literature is rapidly changing and evolving in our understanding of basal sex differences in the brain, as well as the interaction between biological sex and life experiences. The animal literature provides the distinctive opportunity to explore sex-specific stress- and alcohol- induced changes in neurocircuits on a relatively rapid time scale. In addition, animal models allow for the investigation of individual neurons and signaling molecules otherwise inaccessible in the human brain. Here, we review the human and rodent literature with a focus on cortical development, neurotransmitters, peptides, and steroids, to characterize the field’s current understanding of the interaction between adolescence, biological sex, and exposure to stress and alcohol.

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“…Because stress can influence rates of adolescent neurogenesis ( Mouri et al, 2018 ), it is important to characterize the effects of aversive experiences on hippocampal development during the adolescent period for its effect not just during adolescence but into adulthood as well. However, other stress paradigms during adolescence have produced null results on neurogenesis ( Harris et al, 2022 ), and in general there is a lack of knowledge for how different types of stressors of various frequencies and severities impact adolescent neurogenesis. As adolescent stress can impact other forms of structural plasticity ( Eiland and Romeo, 2013 ), the more we understand about how stress impacts the developing hippocampus and rest of the brain, the better we can understand the relative resilience and susceptibility that various stressors have during the adolescent period.…”

Section: Discussionmentioning

confidence: 99%

“…Studies focusing on neurogenesis in the dentate gyrus region of the hippocampus largely find that adolescent stress increases cell proliferation and neurogenesis once in adulthood ( Toth et al, 2008 ; McCormick et al, 2012 ). However, the few studies that measure the effects of stress on adolescent neurogenesis are mixed ( Mouri et al, 2018 ; Harris et al, 2022 ). As neurogenesis is substantially higher during adolescence than adulthood ( He and Crews, 2007 ), alterations to adolescent neurogenesis by stress have the potential to strongly alter the late development of the hippocampus and its structure and function into adulthood.…”

Section: Introductionmentioning

confidence: 99%

Inhibition of Hippocampal Neurogenesis Starting in Adolescence Increases Anxiodepressive Behaviors Amid Stress

Larivee

Johnson

Freedgood

et al. 2022

Front. Behav. Neurosci.

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Stressors during the adolescent period can affect development of the brain and have long-lasting impacts on behavior. Specifically, adolescent stress impairs hippocampal neurogenesis and can increase risk for anxiety, depression, and a dysregulated stress response in adulthood. In order to model the functional effects of reduced hippocampal neurogenesis during adolescence, a transgenic neurogenesis ablation rat model was used to suppress neurogenesis during the adolescent period and test anxiodepressive behaviors and stress physiology during adulthood. Wildtype and transgenic (TK) rats were given valganciclovir during the first two weeks of adolescence (4-6 weeks old) to knock down neurogenesis in TK rats. Starting in young adulthood (13 weeks old), blood was sampled for corticosterone at several time points following acute restraint stress to measure negative feedback of the stress response, and rats were tested on a battery of anxiodepressive tests at baseline and following acute restraint stress. Although TK rats had large reductions in both cell proliferation during adolescence, as measured by bromodeoxyuridine (BrdU), and ongoing neurogenesis in adulthood (by doublecortin), resulting in decreased volume of the dentate gyrus, negative feedback of the stress response following acute restraint was similar across all rats. Despite similar stress responses, TK rats showed higher anxiety-like behavior at baseline. In addition, only TK rats had increased depressive-like behavior when tested after acute stress. Together, these results suggest that long-term neurogenesis ablation starting in adolescence produces hippocampal atrophy and increases behavioral caution and despair amid stressful environments.

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Juvenile stress exerts sex-independent effects on anxiety, antidepressant-like behaviours and dopaminergic innervation of the prelimbic cortex in adulthood and does not alter hippocampal neurogenesis

Cited by 7 publications

References 106 publications

Protective Effects of Resveratrol on Adolescent Social Isolation-Induced Anxiety-Like Behaviors via Modulating Nucleus Accumbens Spine Plasticity and Mitochondrial Function in Female Rats

Protective Effects of Resveratrol on Adolescent Social Isolation-Induced Anxiety-Like Behaviors via Modulating Nucleus Accumbens Spine Plasticity and Mitochondrial Function in Female Rats

Adolescent Alcohol and Stress Exposure Rewires Key Cortical Neurocircuitry

Inhibition of Hippocampal Neurogenesis Starting in Adolescence Increases Anxiodepressive Behaviors Amid Stress

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