Prefrontal Plasticity and Stress Inoculation-Induced Resilience

Katz, Maor; Liu, Chunlei; Schaer, Marie; Parker, Karen J.; Ottet, Marie-Christine; Epps, Averi; Buckmaster, Christine L.; Bammer, Roland; Moseley, Michael E.; Schatzberg, Alan F.; Eliez, Stéphan; Lyons, David M.

doi:10.1159/000216540

Cited by 79 publications

(82 citation statements)

References 118 publications

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“…Operationalizing early moderate stressors as involving temporary removal from the natal group, one study (Parker, Buckmaster, Justus, Schatzberg, & Lyons, 2005) found evidence of better performance in this condition than in the non-stressed condition on a later cognitive control task. Consistent with this finding, moderate stressors experimentally induced using this paradigm are associated with greater prefrontal myelination and larger ventromedial prefrontal cortices (Katz et al, 2009), areas of the brain that have been associated with poorer decision-making and reduced activation in suicidal individuals (Bridge et al, 2012; Currier & Mann, 2008; van Heeringen, Bijttebier, & Godfrin, 2011). …”

Section: Empirical Findingssupporting

confidence: 61%

A developmentally informed perspective on the relation between stress and psychopathology: When the problem with stress is that there is not enough.

Liu¹

2015

Journal of Abnormal Psychology

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A common tenet of several prominent theories of stress and psychopathology (e.g., stress exposure) is that experiencing high rates of life stressors is associated with greater risk for negative mental health outcomes. Although there has been substantial empirical support for this position, another possibility that has received considerably less attention to date is that early life stressors may share a curvilinear rather than monotonic relation with psychological well-being. In what has been termed the “steeling effect,” “stress inoculation,” and “antifragility,” exposure to moderate stressors early in life may confer resilience to potential detrimental effects of later stressors. An interesting implication of this model is that low levels of early life stressors, relative to normatively moderate rates, may be associated with greater sensitivity to future stressors. The present paper reviews preliminary evidence consistent with this possibility, drawing on behavioral and neurobiological studies in animal models, and the more modest literature on neurocognitive, psychological, and psychophysiological functioning in humans. Limitations of the clinical literature and possible directions for future research are discussed, including naturalistic longitudinal studies with clinical outcomes, and for research examining moderators and mechanisms, across multiple levels of analysis (e.g., cognitive, immunological, and neurobiological).

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Section: Empirical Findingssupporting

confidence: 61%

A developmentally informed perspective on the relation between stress and psychopathology: When the problem with stress is that there is not enough.

Liu¹

2015

Journal of Abnormal Psychology

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“…Optogenetic stimulation of vmPFC neurons reverses depression-like behavior in mice susceptible to chronic social defeat stress [40]. Brief maternal separation in squirrel monkeys promotes stress inoculation and increases cortical volume in the vmPFC [41]. Also, neural activity in the vmPFC is both necessary and sufficient for the resistance to learned helplessness conferred by prior experience with controllable stress [18, 19, 42].…”

Section: Discussionmentioning

confidence: 99%

Maintenance of dominance status is necessary for resistance to social defeat stress in Syrian hamsters

Morrison

Bader

Clinard

et al. 2014

Behavioural Brain Research

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Resilience is an active process that involves a discrete set of neural substrates and cellular mechanisms and enables individuals to avoid some of the negative consequences of extreme stress. We have previously shown that dominant individuals show less stress-induced changes in behavior compared to subordinates using a conditioned defeat model in male Syrian hamsters (Mesocricetus auratus). To rule out pre-existing differences between dominants and subordinates, we examined whether 14 days of dominance experience is required to reduce the conditioned defeat response and whether the development of conditioned defeat resistance correlates with defeat-induced neural activation in select brain regions. We paired hamsters in daily 5-min aggressive encounters for 1, 7, or 14 days and then exposed animals to 3, 5-min social defeat episodes. The next day animals received conditioned defeat testing which involved a 5-min social interaction test with a non-aggressive intruder. In separate animals brains were collected after social defeat for c-Fos immunohistochemistry. We found that 14-day dominants showed a decreased conditioned defeat response compared to 14-day subordinates and controls, while 1-day and 7-day dominants did not differ from their subordinate counterparts. Also, the duration of dominance relationship was associated with distinct patterns of defeat-induced neural activation such that only 14-day dominants showed elevated c-Fos immunoreactivity in the ventral medial prefrontal cortex, medial amygdala, and lateral portions of the ventral medial hypothalamus. Our data suggest that resistance to social stress develops during the maintenance of dominance relationships and is associated with experience-dependent neural plasticity in select brain regions.

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“…Novelty seeking was also assessed in NS and SI squirrel monkeys at 2.5 years of age (Parker et al., 2007). Magnetic resonance imaging (MRI) of brain was conducted with NS and SI squirrel monkeys at 3.3 years of age (Katz et al., 2009) and place preference conditioning tests of NS and SI squirrel monkeys were conducted at 4.4 years of age (unpublished observations). Cognitive control, novelty seeking, place preference conditioning, and previous neuroimaging procedures were not conducted with SI + Mom squirrel monkeys and provided the opportunity to assess stress inoculation versus subsequent testing effects.…”

Section: Methodsmentioning

confidence: 99%

Striatal dopamine D2/3 receptor regulation by stress inoculation in squirrel monkeys

Lee

Nechvatal

Shen

et al. 2016

Neurobiology of Stress

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Intermittent mildly stressful situations provide opportunities to learn, practice, and improve coping in a process called stress inoculation. Stress inoculation also enhances cognitive control and response inhibition of impulsive motivated behavior. Cognitive control and motivation have been linked to striatal dopamine D2 and/or D3 receptors (DRD2/3) in rodents, monkeys, and humans. Here, we study squirrel monkeys randomized early in life to stress inoculation with or without maternal companionship and a no-stress control treatment condition. Striatal DRD2/3 availability in adulthood was measured in vivo by [11C]raclopride binding using positron emission tomography (PET). DRD2/3 availability was greater in caudate and putamen compared to ventral striatum as reported in PET studies of humans and other non-human primates. DRD2/3 availability in ventral striatum was also consistently greater in stress inoculated squirrel monkeys compared to no-stress controls. Squirrel monkeys exposed to stress inoculation in the presence of their mother did not differ from squirrel monkeys exposed to stress inoculation without maternal companionship. Similar effects in different social contexts extend the generality of our findings and together suggest that stress inoculation increases striatal DRD2/3 availability as a correlate of cognitive control in squirrel monkeys.

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Prefrontal Plasticity and Stress Inoculation-Induced Resilience

Cited by 79 publications

References 118 publications

A developmentally informed perspective on the relation between stress and psychopathology: When the problem with stress is that there is not enough.

A developmentally informed perspective on the relation between stress and psychopathology: When the problem with stress is that there is not enough.

Maintenance of dominance status is necessary for resistance to social defeat stress in Syrian hamsters

Striatal dopamine D2/3 receptor regulation by stress inoculation in squirrel monkeys

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