Stress-elicited neural activity in young adults varies with childhood sexual abuse

Purcell, Juliann B.; Goodman, Adam M.; Harnett, Nathaniel G.; Davis, Elizabeth; Wheelock, Muriah D.; Mrug, Sylvie; Elliott, Marc N.; Emery, Susan Tortolero; Schuster, Mark A.; Knight, David C.

doi:10.1016/j.cortex.2020.12.020

Cited by 9 publications

(13 citation statements)

References 99 publications

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“…The extent to which these rodent behavioral changes reflect those observed in victims of early sexual abuse in humans remains unknown, but it may be relevant that childhood sexual abuse has been associated with reduced cognitive function ( Navalta et al, 2006 ) as well as impaired parenting skills ( Burkett, 1991 ; Cole et al, 1992 ; Ethier et al, 1995 ). Very limited evidence exists regarding the effects of this paradigm on the rodent brain, but available data suggest a reduction in neuronal growth in the hippocampus ( Shors et al, 2016 ), which is consistent with work in humans showing that hippocampal volume and activation are reduced after childhood sexual abuse ( Weniger et al, 2008 ; Yuan et al, 2020 ; Purcell et al, 2021 ; compare Table 2 with Table 1 ). Clearly, this approach presents an innovative experimental animal paradigm that should be explored further for potential translational relevance.…”

Section: Sexual Aggressionsupporting

confidence: 70%

“…Childhood sexual and physical abuse have been linked to reduced volume of the amygdala regardless of clinical diagnosis ( Nogovitsyn et al, 2020 ) suggesting that early exposure to trauma alters the structural development of this region, perhaps contributing to vulnerability to subsequent stress. Childhood sexual, but not physical, abuse has been associated with diminished stress-induced activation of the dorsolateral frontal cortex and hippocampus ( Purcell et al, 2021 ). Childhood sexual abuse produces thinning of the visual cortex and somatosensory cortex associated with genital representations in a way that may not be related to the development of psychopathology as the effects can be observed even in individuals without diagnoses ( Tomoda et al, 2009 ; Heim et al, 2013 ).…”

Section: Sexual Abusementioning

confidence: 99%

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

Waters

Gould

2022

Front. Syst. Neurosci.

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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.

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Section: Sexual Aggressionsupporting

confidence: 70%

Section: Sexual Abusementioning

confidence: 99%

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

Waters

Gould

2022

Front. Syst. Neurosci.

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“…Thus, changes in hippocampal structure may partially underlie the disruptions in memory function that are associated with alcohol use. The hippocampus also plays an important role in emotion expression and regulation (Ghasemi et al, 2022; Hartley & Phelps, 2010; Purcell et al, 2021; Snyder et al, 2011). For example, the hippocampus supports the extinction of conditioned fear, and alterations in hippocampal function have been linked to anxiety-related conditions (e.g., posttraumatic stress disorder, panic disorders; Ghasemi et al, 2022; Hartley & Phelps, 2010; Knight et al, 2004).…”

Section: Discussionmentioning

confidence: 99%

Hippocampal gray matter volume in young adulthood varies with adolescent alcohol use.

Purcell,

Harnett,

Mrug

et al. 2024

Experimental and Clinical Psychopharmacology

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Adolescent substance use is linked with negative future outcomes (e.g., depression, anxiety, substance use disorder). Given that the brain undergoes significant maturation during adolescence, this developmental period may represent a time of particular vulnerability to substance use. Neuroimaging research has largely focused on heavy or binge patterns of substance use; thus, relatively less is known about the neural impact of a broader range of adolescent substance use. Characterizing the neural impact of a broader range of adolescent substance use may inform prevention and treatment efforts. The present study investigated relationships between adolescent substance use trajectories (i.e., alcohol, tobacco, and cannabis) and gray matter volume in young adulthood. Substance use was assessed in 1,594 participants at ages 11, 13, 16, and 19. Following the last assessment, 320 participants completed a single magnetic resonance imaging session to assess brain gray matter volume. Latent growth curve models were used to estimate growth parameters characterizing alcohol, tobacco, and cannabis use trajectories for each participant. These growth parameters (i.e., intercept, linear slope, and quadratic slope) were then used as predictors of gray matter volume. The gray matter volume of the hippocampus was positively associated with age 14 alcohol use (i.e., intercept) but not other trajectories (i.e., progression or acceleration) or substances (tobacco or cannabis). These results provide new insight into the neural impact of distinct adolescent alcohol, tobacco, and cannabis use trajectories, which may help to refine prevention and treatment efforts.

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“…Prior neuroimaging findings revealed that MDD patients exhibited altered neural stress response in limbic‐striatal‐prefrontal regions (Admon et al, 2015; Holsen et al, 2011; Ming et al, 2017). Moreover, neuroimaging studies in healthy individuals reported that CM is associated with increased stress‐induced activation in the amygdala (Grimm et al, 2014; Seo et al, 2019), hippocampus (Grimm et al, 2014; Seo et al, 2019), anterior cingulate cortex (Grimm et al, 2014), dorsal medial prefrontal cortex (mPFC; van Harmelen et al, 2014), cerebellum (Seo et al, 2019), medial temporal lobe (Seo et al, 2019), insula (Zhong et al, 2020), precuneus (Zhong et al, 2020), and decreased stress‐induced activation in the ventromedial and dorsolateral prefrontal cortex (Purcell et al, 2021), as well as increased stress‐induced amygdala‐hippocampus connectivity (Fan et al, 2015). Although these findings are not always consistent, they suggest that CM may impact neural stress responses in neural circuitries partly overlapping with regions consistently implicated in MDD (e.g., amygdala, hippocampus, and prefrontal cortex).…”

Section: Introductionmentioning

confidence: 99%

“…Moreover, neuroimaging studies in healthy individuals reported that CM is associated with increased stress-induced activation in the amygdala (Grimm et al, 2014;Seo et al, 2019), hippocampus (Grimm et al, 2014;Seo et al, 2019), anterior cingulate cortex (Grimm et al, 2014), dorsal medial prefrontal cortex (mPFC; van Harmelen et al, 2014), cerebellum (Seo et al, 2019), medial temporal lobe (Seo et al, 2019), insula (Zhong et al, 2020), precuneus (Zhong et al, 2020), and decreased stress-induced activation in the ventromedial and dorsolateral prefrontal cortex (Purcell et al, 2021), as well as increased stress-induced amygdala-hippocampus connectivity (Fan et al, 2015).…”

mentioning

confidence: 99%

Distinct stress‐related medial prefrontal cortex activation in women with depression with and without childhood maltreatment

Dong

Belleau

Ironside

et al. 2022

Depression and Anxiety

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Background Emerging evidence has highlighted the moderating effect of childhood maltreatment (CM) in shaping neurobiological abnormalities in major depressive disorder (MDD). However, whether neural mechanisms underlying stress sensitivity in MDD are affected by the history of CM is unclear. Methods Two hundred and thirteen medication‐free female participants were recruited for a functional magnetic resonance imaging study assessing the effects of psychosocial stress on neural responses. The Montreal Imaging Stress Task was administrated to 44 female MDD patients with CM (MDD/CM), 32 female MDD patients without CM (MDD/noCM), 43 female healthy controls (HCs) with CM (HC/CM), and 94 female HCs without CM (HC/noCM). A CM (CM, noCM) × diagnosis (MDD, HC) whole‐brain voxel‐wise analysis was run to assess putative group differences in neural stress responses. Results A significant CM × Diagnosis interaction emerged in the medial prefrontal cortex (mPFC). Bonferroni‐corrected simple effects analysis clarified that (1) the MDD/CM group had less mPFC deactivation than the HC/CM group, (2) the MDD/noCM group exhibited greater mPFC deactivation than the HC/noCM group, and (3) the MDD/CM group exhibited less mPFC deactivation relative to the MDD/noCM group. In addition, the mPFC‐seed psychophysiological interaction analysis revealed that individuals in the CM groups had significantly greater stress‐related mPFC‐left superior frontal gyrus and mPFC‐right posterior cerebellum connectivity relative to the noCM groups. Conclusions Findings highlight distinct neural abnormalities in MDD depending on prior CM history, particularly potentiated stress‐related mPFC recruitment among MDD individuals reporting CM. Moreover, CM history was generally associated with the disruption in functional connectivity centered on the mPFC.

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Stress-elicited neural activity in young adults varies with childhood sexual abuse

Cited by 9 publications

References 99 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

Hippocampal gray matter volume in young adulthood varies with adolescent alcohol use.

Distinct stress‐related medial prefrontal cortex activation in women with depression with and without childhood maltreatment

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