Early life social stress and resting state functional connectivity in postpartum rat anterior cingulate circuits

Nephew, Benjamin C.; Febo, Marcelo; Huang, Wei; Colon-Perez, Luis M.; Payne, Laurellee; Poirier, Guillaume L.; Greene, Owen; King, Jean A.

doi:10.1016/j.jad.2017.12.089

Cited by 18 publications

(15 citation statements)

References 105 publications

(136 reference statements)

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“…Animal evidence for the role of these premotor circuits in inhibiting automatic and enabling intentional responses includes microstimulation of preSMA neurons (Isoda and Hikosaka, 2007 ), and macrostimulation in humans produces similar effects (Swann et al, 2012 ). A rodent paradigm found altered connectivity patterns in prefrontal and motor areas in female rats subjected to chronic social stress as pups (Nephew et al, 2017 , 2018 ). Silvers et al ( 2017 ) found that as typically-developing children reach adulthood, reactivity to aversive relative to neutral stimuli shifted from ventromedial (vmPFC) to dorsomedial prefrontal cortex (dmPFC), including preSMA, whereas Herringa and colleagues (Keding and Herringa, 2016 ; Wolf and Herringa, 2016 ) found a reverse profile of activation and limbic connectivity in children suffering from PTSD.…”

Section: Discussionmentioning

confidence: 99%

Childhood Emotional Abuse Moderates Associations Among Corticomotor White Matter Structure and Stress Neuromodulators in Women With and Without Depression

et al. 2018

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Adverse caregiving during development can produce long-lasting changes to neural, endocrine, and behavioral responses to stress, and is strongly related to elevated risk of adult psychopathology. While prior experience of adversity is associated with altered sympathetic nervous system (SNS) and hypothalamic-pituitary-adrenal (HPA) axis activity, the underlying neural pathways are not completely understood. In a double-blind crossover study, we used diffusion tensor imaging (DTI) to examine whether variation in white matter structure predicts differences in HPA-SNS interactions as a function of early adversity. Participants included 74 women who exhibited a wide range of depression severity and/or childhood emotional abuse (EA). Participants attended two experimental sessions during which they were administered 20 mg cortisol (CORT) or placebo and after 90 min, viewed emotionally laden pictures while undergoing MRI scanning. Immediately after emotional picture-viewing, we collected salivary alpha-amylase (sAA) to index SNS activation. We tested whether EA moderated the relation between fractional anisotropy (FA), a measure of white matter fiber structure, and sAA. In the placebo condition, for participants with minimal history of EA, higher FA in corticomotor projections was negatively correlated with sAA, whereas in participants with severe EA, the correlation was trending in the opposite direction. Following CORT administration, FA and sAA were not related, suggesting that SNS tone during acute cortisol elevation may depend on neural pathways other than corticomotor projections. The results suggest that at baseline—though not during cortisol elevation—increased FA in these tracts is associated with lower levels of SNS activity in women with minimal EA, but not in women with severe EA. These findings provide evidence that corticomotor projections may be a key component of altered neural circuitry in adults with history of maltreatment, and may be related to alterations in stress neuromodulators in psychopathology.

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Section: Discussionmentioning

confidence: 99%

Childhood Emotional Abuse Moderates Associations Among Corticomotor White Matter Structure and Stress Neuromodulators in Women With and Without Depression

et al. 2018

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“…A promising area that has recently gained increasing attention is the environmental conditions experienced by individuals during early-life stages. A well-established body of evidence supports the concept that early-life stress exposure increases the probability of social behaviour deficits manifesting later in life across a range of taxa [30][31][32][33]. For example, early-life stress increased the probability of psychiatric disorders in humans [30] and had adverse effects on social bonding in prairie voles, Microtus ochrogaster [31], and maternal care in rats, Rattus norvegicus domesticus [32].…”

Section: Introductionmentioning

confidence: 94%

Early-life social environment predicts social network position in wild zebra finches

et al. 2019

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Early-life experience can fundamentally shape individual life-history trajectories. Previous research has suggested that exposure to stress during development causes differences in social behaviour later in life. In captivity, juvenile zebra finches exposed to elevated corticosterone levels were less socially choosy and more central in their social networks when compared to untreated siblings. These differences extended to other aspects of social life, with 'stress-exposed' juveniles switching social learning strategies and juvenile males less faithfully learning their father's song. However, while this body of research suggests that the impacts of early-life stress could be profound, it remains unknown whether such effects are strong enough to be expressed under natural conditions. Here, we collected data on social associations of zebra finches in the Australian desert after experimentally manipulating brood sizes. Juveniles from enlarged broods experienced heightened sibling competition, and we predicted that they would express similar patterns of social associations to stress-treated birds in the captive study by having more, but less differentiated, relationships. We show striking support for the suggested consequences of developmental stress on social network positions, with our data from the wild replicating the same results in 9 out of 10 predictions previously tested in captivity. Chicks raised in enlarged broods foraged with greater numbers of conspecifics but were less 'choosy' and more central in the social network. Our results confirm that the natural range of variation in early-life experience can be sufficient to predict individuals' social trajectories and support theory highlighting the potential importance of developmental conditions on behaviour.

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“…This is a segmentation atlas based on the Paxinos and Watson (1998) atlas of the rat brain. It was developed by Ekam imaging (Northeastern University, Boston, MA; Yee et al, 2015) and has been used in a number of previous publications (Febo et al, 2009;Nephew et al, 2009Nephew et al, , 2018Colon-Perez et al, 2018). Signals were averaged from voxels in each ROI (Colon-Perez et al, 2016).…”

Section: Image Processingmentioning

confidence: 99%

Multiscale Imaging Reveals Aberrant Functional Connectome Organization and Elevated Dorsal StriatalArcExpression in Advanced Age

Colon-Perez

Turner

Lubke

et al. 2019

eNeuro

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The functional connectome reflects a network architecture enabling adaptive behavior that becomes vulnerable in advanced age. The cellular mechanisms that contribute to altered functional connectivity in old age, however, are not known. Here we used a multiscale imaging approach to link age-related changes in the functional connectome to altered expression of the activity-dependent immediate-early gene Arc as a function of training to multitask on a working memory (WM)/biconditional association task (BAT). Resting-state fMRI data were collected from young and aged rats longitudinally at three different timepoints during cognitive training. After imaging, rats performed the WM/BAT and were immediately sacrificed to examine expression levels of Arc during task performance. Aged behaviorally impaired, but not young, rats had a subnetwork of increased connectivity between the anterior cingulate cortex (ACC) and dorsal striatum (DS) that was correlated with the use of a suboptimal response-based strategy during cognitive testing. Moreover, while young rats had stable rich-club organization across three scanning sessions, the rich-club organization of old rats increased with cognitive training. In a control group of young and aged rats that were longitudinally scanned at similar time intervals, but without cognitive training, ACC-DS connectivity and rich-club organization did not change between scans in either age group. These findings suggest that aberrant large-scale functional connectivity in aged animals is associated with altered cellular activity patterns within individual brain regions.

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Early life social stress and resting state functional connectivity in postpartum rat anterior cingulate circuits

Abstract: This behavioral and functional neuroanatomical foundation can now be used to enhance our understanding of the neural etiology of early life stress associated disorders and test preventative measures and treatments for stress related disorders.

Cited by 18 publications

References 105 publications

Childhood Emotional Abuse Moderates Associations Among Corticomotor White Matter Structure and Stress Neuromodulators in Women With and Without Depression

Childhood Emotional Abuse Moderates Associations Among Corticomotor White Matter Structure and Stress Neuromodulators in Women With and Without Depression

Early-life social environment predicts social network position in wild zebra finches

Multiscale Imaging Reveals Aberrant Functional Connectome Organization and Elevated Dorsal StriatalArcExpression in Advanced Age

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