Pre-adolescent stress disrupts adult, but not adolescent, safety learning

Meyer, Heidi C.; Gerhard, Danielle M.; Amelio, Paia A.; Lee, Francis S.

doi:10.1016/j.bbr.2020.113005

Cited by 14 publications

(10 citation statements)

References 62 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Additional paradigms have modeled exposure to multiple types of adversity beginning before weaning and extending into adolescence by either combining a more traditional ELA paradigm, like maternal separation, with subsequent exposure to additional stressors in mice and rats ( Huang et al, 2021 ; Knox et al, 2021 ; Saavedra et al, 2021 ), or by subjecting developing mice and rats to different types of stressors ( Yohn and Blendy, 2017 ; Page and Coutellier, 2018 ; Meyer et al, 2021 ). In general, these studies have shown that multiple adversity exposure throughout development increases avoidance behavior as well as impairs stress coping and reward seeking ( Chaby et al, 2015 ; Yohn and Blendy, 2017 ; Page and Coutellier, 2018 ; Huang et al, 2021 ; Knox et al, 2021 ; Meyer et al, 2021 ; Saavedra et al, 2021 ), findings that are generally consistent with the human literature demonstrating a link between multiple ELA exposures not only increasing the risk and severity of neuropsychiatric disease ( Anda et al, 2006 ; Dich et al, 2015 ) but also increasing the likelihood of anxiety/depression comorbidity ( Espejo et al, 2007 ). Multiple hit developmental models have successfully produced behavioral phenotypes consistent with “anxiety-like” and “depressive-like” behavior in both rats and mice, and the overall picture that has emerged suggests similar general behavioral findings in males and females ( Yohn and Blendy, 2017 ; Page and Coutellier, 2018 ; Knox et al, 2021 ; Saavedra et al, 2021 ).…”

Section: Mixed and Multiple Hit Modelsmentioning

confidence: 99%

Early Life Adversity and Neuropsychiatric Disease: Differential Outcomes and Translational Relevance of Rodent Models

Waters

Gould

2022

Front. Syst. Neurosci.

View full text Add to dashboard Cite

It is now well-established that early life adversity (ELA) predisposes individuals to develop several neuropsychiatric conditions, including anxiety disorders, and major depressive disorder. However, ELA is a very broad term, encompassing multiple types of negative childhood experiences, including physical, sexual and emotional abuse, physical and emotional neglect, as well as trauma associated with chronic illness, family separation, natural disasters, accidents, and witnessing a violent crime. Emerging literature suggests that in humans, different types of adverse experiences are more or less likely to produce susceptibilities to certain conditions that involve affective dysfunction. To investigate the driving mechanisms underlying the connection between experience and subsequent disease, neuroscientists have developed several rodent models of ELA, including pain exposure, maternal deprivation, and limited resources. These studies have also shown that different types of ELA paradigms produce different but somewhat overlapping behavioral phenotypes. In this review, we first investigate the types of ELA that may be driving different neuropsychiatric outcomes and brain changes in humans. We next evaluate whether rodent models of ELA can provide translationally relevant information regarding links between specific types of experience and changes in neural circuits underlying dysfunction.

show abstract

Section: Mixed and Multiple Hit Modelsmentioning

confidence: 99%

Early Life Adversity and Neuropsychiatric Disease: Differential Outcomes and Translational Relevance of Rodent Models

Waters

Gould

2022

Front. Syst. Neurosci.

View full text Add to dashboard Cite

show abstract

“…Sex specific effect is also reported for Wistar rats, when acute stress during adolescence increases anxiety behavior in male Sprague-Dawley rats, while females are not affected ( Lovelock and Deak, 2019 ). Most studies report increased anxiety-like behaviors in adult male rodents after a single or repeated mild stress during the same developmental period ( Tsoory et al, 2007 ; Mancini et al, 2021 ; Meyer et al, 2021 ). In contrast, a 3-day stress in the same EA period increases anxiety-like measures in the OFT and the EPM in both adult male and female rats ( Jacobson-Pick and Richter-Levin, 2010 ).…”

Section: Discussionmentioning

confidence: 99%

“…Most studies report increased anxiety-like behaviors in adult male rodents after a single or repeated mild stress during the same developmental period (Tsoory et al, 2007;Mancini et al, 2021;Meyer et al, 2021). In contrast, a 3-day stress in the same EA period increases anxiety-like measures in the OFT and the EPM in both adult male and female rats (Jacobson-Pick and Richter-Levin, 2010).…”

Section: Discussionmentioning

confidence: 99%

Sex-Specific Behavioral Response to Early Adolescent Stress in the Genetically More Stress-Reactive Wistar Kyoto More Immobile, and Its Nearly Isogenic Wistar Kyoto Less Immobile Control Strain

Kim

Gacek

Mocchi

et al. 2021

Front. Behav. Neurosci.

View full text Add to dashboard Cite

Genetic predisposition and environmental stress are known etiologies of stress-related psychiatric disorders. Environmental stress during adolescence is assumed to be particularly detrimental for adult affective behaviors. To investigate how genetic stress-reactivity differences modify the effects of stress during adolescence on adult affective behaviors we employed two inbred strains with differing stress reactivity. The Wistar Kyoto More Immobile (WMI) rat strain show increased stress-reactivity and despair-like behaviors as well as passive coping compared to the nearly isogenic control strain, the Wistar Kyoto Less Immobile (WLI). Males and females of these strains were exposed to contextual fear conditioning (CFC) during early adolescence (EA), between 32 and 34 postnatal days (PND), and were tested for the consequences of this mild EA stress in adulthood. Early adolescent stress significantly decreased anxiety-like behavior, measured in the open field test (OFT) and increased social interaction and recognition in adult males of both strains compared to controls. In contrast, no significant effects of EA stress were observed in adult females in these behaviors. Both males and females of the genetically less stress-reactive WLI strain showed significantly increased immobility in the forced swim test (FST) after EA stress compared to controls. In contrast, immobility was significantly attenuated by EA stress in adult WMI females compared to controls. Transcriptomic changes of the glucocorticoid receptor (Nr3c1, GR) and the brain-derived neurotrophic factor (Bdnf) illuminate primarily strain and stress-dependent changes, respectively, in the prefrontal cortex and hippocampus of adults. These results suggest that contrary to expectations, limited adolescent stress is beneficial to males thru decreasing anxiety and enhancing social behaviors, and to the stress more-reactive WMI females by way of decreasing passive coping.

show abstract

“…Importantly, whereas stress disrupts extinction learning, recent evidence in rodents suggests that safety signals may be a robust approach to fear reduction even following stress—rodents exposed to prior stress showed impaired fear extinction, but no disruption in conditioned inhibition 26 . Moreover, evidence in rodents suggests that adolescence may be a unique period when conditioned inhibition is robust to effects of stress experienced in childhood 27 . These findings suggest that safety signal learning could target an alternative neural circuit to promote resilience beyond traditional extinction-based approaches during adolescence.…”

Section: Reducing Fear Via Safety Signal Learningmentioning

confidence: 99%

Leveraging the science of stress to promote resilience and optimize mental health interventions during adolescence

et al. 2022

View full text Add to dashboard Cite

show abstract

Pre-adolescent stress disrupts adult, but not adolescent, safety learning

Cited by 14 publications

References 62 publications

Early Life Adversity and Neuropsychiatric Disease: Differential Outcomes and Translational Relevance of Rodent Models

Early Life Adversity and Neuropsychiatric Disease: Differential Outcomes and Translational Relevance of Rodent Models

Sex-Specific Behavioral Response to Early Adolescent Stress in the Genetically More Stress-Reactive Wistar Kyoto More Immobile, and Its Nearly Isogenic Wistar Kyoto Less Immobile Control Strain

Leveraging the science of stress to promote resilience and optimize mental health interventions during adolescence

Contact Info

Product

Resources

About