Maternal Style Selectively Shapes Amygdalar Development and Social Behavior in Rats Genetically Prone to High Anxiety

Cohen, Joshua L.; Glover, Matthew E.; Pugh, Phyllis C.; Fant, Andrew D.; Simmons, Rebecca K.; Akil, Huda; Kerman, Ilan A.; Clinton, Sarah M.

doi:10.1159/000374108

Cited by 34 publications

(58 citation statements)

References 52 publications

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“…highly exploratory and impulsive) vs. low responders (LH; e.g. heightened anxiety- and depressive-like behavior), cross-fostering at birth between HR and LR results in reduced anxiety-like behavior and altered gene expression in the amygdala of LR offspring reared by HR dams [139]. In mice selectively bred for alcohol preference [high alcohol preference (HAP) vs. low alcohol preference (LAP)], cross-fostering at birth indicates that HAP pups reared by LAP dams have reduced levels of alcohol preference.…”

Section: Timing and Sensitive Periodsmentioning

confidence: 99%

Influence of maternal care on the developing brain: Mechanisms, temporal dynamics and sensitive periods

Curley

Champagne

2016

Frontiers in Neuroendocrinology

209

117

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Variation in maternal care can lead to divergent developmental trajectories in offspring with implications for neuroendocrine function and behavioral phenotypes. Study of the long-term outcomes associated with mother-infant interactions suggests complex mechanisms linking the experience of variation in maternal care and these neurobiological consequences. Through integration of genetic, molecular, cellular, neuroanatomical, and neuroendocrine approaches, significant advances in our understanding of these complex pathways have been achieved. In this review, we will consider the impact of maternal care on male and female offspring development with a particular focus on the issues of timing and mechanism. Identifying the period of sensitivity to maternal care and the temporal dynamics of the molecular and neuroendocrine changes that are a consequence of maternal care represents a critical step in the study of mechanism.

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Section: Timing and Sensitive Periodsmentioning

confidence: 99%

Influence of maternal care on the developing brain: Mechanisms, temporal dynamics and sensitive periods

Curley

Champagne

2016

Frontiers in Neuroendocrinology

209

117

View full text Add to dashboard Cite

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“…Sprague Dawley rats that were selectively bred to display low behavioral response to novelty (Low Responders, LR) also exhibit high anxiety- and depression-like behavior compared to High Novelty Responder rats (HRs). These behaviors include diminished sociability and sexual motivation, increased behavioral inhibition and helplessness, as well as greater vulnerability to chronic stress (Stead et al, 2006a, Stedenfeld et al, 2011, Cummings et al, 2013, Clinton et al, 2014, Cohen et al, 2015). Furthermore, these behavioral traits emerge in early life, and a previous microarray study from our group revealed widespread gene expression differences in the early postnatal HR versus LR brain (Clinton et al, 2011).…”

Section: Introductionmentioning

confidence: 99%

“…Our previous work suggested that HR/LR differences in anxiety/depression-like behavior stem from disparate developmental trajectories in the early postnatal hippocampus and possibly amygdala (Clinton et al, 2011, Cohen et al, 2015). These early life HR/LR gene expression differences involved several functional classes of genes, including those relevant to synaptogenesis, synaptic plasticity, and cellular metabolism.…”

Section: Introductionmentioning

confidence: 99%

Altered metabolic activity in the developing brain of rats predisposed to high versus low depression-like behavior

et al. 2016

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Individual differences in human temperament can increase risk for psychiatric disorders like depression and anxiety. Our laboratory utilized a rat model of temperamental differences to assess neurodevelopmental factors underlying emotional behavior differences. Rats selectively bred for low novelty exploration (Low Responders, LR) display high levels of anxiety- and depression-like behavior compared to High Novelty Responder (HR) rats. Using transcriptome profiling, the present study uncovered vast gene expression differences in the early postnatal HR versus LR limbic brain, including changes in genes involved in cellular metabolism. These data led us to hypothesize that rats prone to high (versus low) anxiety/depression-like behavior exhibit distinct patterns of brain metabolism during the first weeks of life, which may reflect disparate patterns of synaptogenesis and brain circuit development. Thus, in a second experiment we examined activity of Cytochrome C Oxidase (COX), an enzyme responsible for ATP production and a correlate of metabolic activity, to explore functional energetic differences in HR/LR early postnatal brain. We found that HR rats display higher COX activity in the amygdala and specific hippocampal subregions compared to LRs during the first 2 weeks of life. Correlational analysis examining COX levels across several brain regions and multiple early postnatal time points suggested desynchronization in the developmental timeline of the limbic HR versus LR brain during the first two postnatal weeks. These early divergent COX activity levels may reflect altered circuitry or synaptic activity in the early postnatal HR/LR brain, which could contribute to the emergence of their distinct behavioral phenotypes.

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“…Finally, hypoglycemia is a potent stressor and leads to robust corticosterone response in three-week-old rats [51]. Early life stress negatively influences regional gene expression and behavioral performance, and is known to suppress BDNF expression in the PFC [52–55]. Future studies are necessary to address all these possibilities.…”

Section: Discussionmentioning

confidence: 99%

Recurrent Moderate Hypoglycemia Suppresses Brain-Derived Neurotrophic Factor Expression in the Prefrontal Cortex and Impairs Sensorimotor Gating in the Posthypoglycemic Period in Young Rats

Rao

Ennis

Mitchell³

et al. 2016

Dev Neurosci

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Recurrent hypoglycemia is common in infants and children. In developing rat models, recurrent moderate hypoglycemia leads to neuronal injury in the medial prefrontal cortex. To understand the effects beyond neuronal injury, 3-week-old male rats were subjected to 5 episodes of moderate hypoglycemia (blood glucose concentration, approx. 30 mg/dl for 90 min) once daily from postnatal day 24 to 28. Neuronal injury was determined using Fluoro-Jade B histochemistry on postnatal day 29. The effects on brain-derived neurotrophic factor (BDNF) and its cognate receptor, tyrosine kinase receptor B (TrkB) expression, which is critical for prefrontal cortex development, were determined on postnatal day 29 and at adulthood. The effects on prefrontal cortex-mediated function were determined by assessing the prepulse inhibition of the acoustic startle reflex on postnatal day 29 and 2 weeks later, and by testing for fear-potentiated startle at adulthood. Recurrent hypoglycemia led to neuronal injury confined primarily to the medial prefrontal cortex. BDNF/TrkB expression in the prefrontal cortex was suppressed on postnatal day 29 and was accompanied by lower prepulse inhibition, suggesting impaired sensorimotor gating. Following the cessation of recurrent hypoglycemia, the prepulse inhibition had recovered at 2 weeks. BDNF/TrkB expression in the prefrontal cortex had normalized and fear-potentiated startle was intact at adulthood. Recurrent moderate hypoglycemia during development has significant adverse effects on the prefrontal cortex in the posthypoglycemic period.

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Maternal Style Selectively Shapes Amygdalar Development and Social Behavior in Rats Genetically Prone to High Anxiety

Cited by 34 publications

References 52 publications

Influence of maternal care on the developing brain: Mechanisms, temporal dynamics and sensitive periods

Influence of maternal care on the developing brain: Mechanisms, temporal dynamics and sensitive periods

Altered metabolic activity in the developing brain of rats predisposed to high versus low depression-like behavior

Recurrent Moderate Hypoglycemia Suppresses Brain-Derived Neurotrophic Factor Expression in the Prefrontal Cortex and Impairs Sensorimotor Gating in the Posthypoglycemic Period in Young Rats

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