Multigenerational prenatal stress increases the coherence of brain signaling among cortico–striatal–limbic circuits in adult rats

Skelin, Ivan; Needham, Maurice; Molina, Layla; Metz, Gerlinde A. S.; Gruber, Aaron J.

doi:10.1016/j.neuroscience.2015.01.009

Cited by 15 publications

(12 citation statements)

References 65 publications

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“…In pregnant female rats of three successive generations exposed to prenatal stress, each additional generation of prenatal stress incrementally elevated HPA axis activation and increased anxiety‐like and aversive behaviors in adult female offspring (McCreary, Truica et al., ). Changes in brain signaling reflecting a simplification of network processing in multigenerationally, prenatally stressed rats support the hypothesis that recurrent ancestral stress leads to adaptations in the brain that are different from those caused by single‐generation prenatal stress (Skelin, Needham, Molina, Metz, & Gruber, ). Stress across generations in rats also gradually reduced gestational length, maternal weight gain and behavioral activity, and increased blood glucose levels, with each successive generation (Yao et al., ).…”

Section: Intergenerational Epigenetic Transmission In Humanssupporting

confidence: 55%

Research Review: Intergenerational transmission of disadvantage: epigenetics and parents' childhoods as the first exposure

Scorza

Duarte

Hipwell

et al. 2018

Child Psychology Psychiatry

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Section: Intergenerational Epigenetic Transmission In Humanssupporting

confidence: 55%

Research Review: Intergenerational transmission of disadvantage: epigenetics and parents' childhoods as the first exposure

Scorza

Duarte

Hipwell

et al. 2018

Child Psychology Psychiatry

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“…Moreover, MPS can generate new behavioral traits and a hemispheric dominance shift in the adult F4 generation (Ambeskovic et al, 2017). These changes in multigenerationally stressed offspring parallels simplification of neuronal network processing patterns and improved coherence of brain signaling among cortico-striatal-limbic circuits (Skelin et al, 2015). While the design of the present study does not allow to draw mechanistic conclusions on potential stress resilience, it is possible that epigenetic inheritance of behavioral phenotype (Crews et al, 2012; Zucchi et al, 2012; Gapp et al, 2014a; Yao et al, 2014) may provide a means by which adaptive physiological and emotional responses may be promoted.…”

Section: Discussionmentioning

confidence: 99%

“…In the multigenerational stress lineage, the pregnant parental (F0) generation, their pregnant F1 daughters, F2 granddaughters and F3 great-granddaughters were stressed during pregnancy (Erickson et al, 2014; Yao et al, 2014; Skelin et al, 2015). A lineage of yoked controls was bred with each generation.…”

Section: Methodsmentioning

confidence: 99%

“…As opposed to stress vulnerability, a continuously stressful environment may favor the development of stress tolerance or resilience. Repeated generational PS exposure gradually promotes the formation of new behavioral traits (Ambeskovic et al, 2017) and coherence between brain areas (Skelin et al, 2015). The extent to which cumulative effects of multigenerational PS (MPS) can promote stress resilience, especially in generally more resilient females, has not yet been studied.…”

Section: Introductionmentioning

confidence: 99%

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Evidence for Ancestral Programming of Resilience in a Two-Hit Stress Model

Faraji

Soltanpour

Ambeskovic

et al. 2017

Front. Behav. Neurosci.

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In a continuously stressful environment, the effects of recurrent prenatal stress (PS) may accumulate across generations and alter stress vulnerability and resilience. Here, we report in female rats that a family history of recurrent ancestral PS facilitates certain aspects of movement performance, and that these benefits are abolished by the experience of a second hit, induced by a silent ischemia during adulthood. Female F4-generation rats with and without a family history of cumulative multigenerational PS (MPS) were tested for skilled motor function before and after the induction of a minor ischemic insult by endothelin-1 infusion into the primary motor cortex. MPS resulted in improved skilled motor abilities and blunted hypothalamic-pituitary-adrenal (HPA) axis function compared to non-stressed rats. Deep sequencing revealed downregulation of miR-708 in MPS rats along with upregulation of its predicted target genes Mapk10 and Rasd2. Through miR-708 stress may regulate mitogen-activated protein kinase (MAPK) pathway activity. Hair trace elemental analysis revealed an increased Na/K ratio, which suggests a chronic shift in adrenal gland function. The ischemic lesion activated the HPA axis in MPS rats only; the lesion, however, abolished the advantage of MPS in skilled reaching. The findings indicate that MPS generates adaptive flexibility in movement, which is challenged by a second stressor, such as a neuropathological condition. Thus, a second “hit” by a stressor may limit behavioral flexibility and neural plasticity associated with ancestral stress.

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“…HPC) and animal behaviour, although the effects of multigenerational stress in brain circuits are not well understood 78 . We believe repeated functional assessment using optogenetic 79 and imaging tools 80–82 combined with animal behaviour is ideally suited to monitor in real time the process by which multigenerational stress changes the structure and function of different brain circuits.…”

Section: Discussionmentioning

confidence: 99%

Lack of Social Support Raises Stress Vulnerability in Rats with a History of Ancestral Stress

Faraji

Soltanpour

Lotfi

et al. 2017

Sci Rep

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Stress is a primary risk factor for psychiatric disorders. However, it is not fully understood why some stressed individuals are more vulnerable to psychiatric disorders than others. Here, we investigated whether multigenerational ancestral stress produces phenotypes that are sensitive to depression-like symptoms in rats. We also examined whether social isolation reveals potentially latent sensitivity to depression-like behaviours. F4 female rats born to a lineage of stressed mothers (F0-F3) received stress in adulthood while housed in pairs or alone. Social isolation during stress induced cognitive and psychomotor retardation only in rats exposed to ancestral stress. Social isolation also hampered the resilience of the hypothalamic-pituitary-adrenal axis to chronic stress and reduced hippocampal volume and brain-derived neurotrophic factor (BDNF) expression. Thus, synergy between social isolation and stress may unmask a latent history of ancestral stress, and raises vulnerability to mental health conditions. The findings support the notion that social support critically promotes stress coping and resilience.

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Multigenerational prenatal stress increases the coherence of brain signaling among cortico–striatal–limbic circuits in adult rats

Cited by 15 publications

References 65 publications

Research Review: Intergenerational transmission of disadvantage: epigenetics and parents' childhoods as the first exposure

Research Review: Intergenerational transmission of disadvantage: epigenetics and parents' childhoods as the first exposure

Evidence for Ancestral Programming of Resilience in a Two-Hit Stress Model

Lack of Social Support Raises Stress Vulnerability in Rats with a History of Ancestral Stress

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