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A two-hit adversity model in developing rats reveals sex-specific impacts on prefrontal cortex structure and behavior

View ORCID ProfileKelsea R. Gildawie, Lilly M. Ryll, Jessica C. Hexter, Shayna Peterzell, View ORCID ProfileAlissa A. Valentine, View ORCID ProfileHeather C. Brenhouse
doi: https://doi.org/10.1101/2020.10.23.352161
Kelsea R. Gildawie
Department of Psychology, Northeastern University, Boston, MA, USA
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Lilly M. Ryll
Department of Psychology, Northeastern University, Boston, MA, USA
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Jessica C. Hexter
Department of Psychology, Northeastern University, Boston, MA, USA
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Shayna Peterzell
Department of Psychology, Northeastern University, Boston, MA, USA
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Alissa A. Valentine
Department of Psychology, Northeastern University, Boston, MA, USA
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Heather C. Brenhouse
Department of Psychology, Northeastern University, Boston, MA, USA
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  • For correspondence: h.brenhouse@northeastern.edu
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Abstract

Adversity early in life substantially impacts prefrontal cortex (PFC) development and vulnerability to later-life psychopathology. Importantly, repeated adverse experiences throughout childhood increase the risk for PFC-mediated behavioral deficits more commonly in women. Evidence from animal models points to effects of adversity on later-life neural and behavioral dysfunction; however, few studies have investigated the neurobiological underpinnings of sex-specific, long term consequences of multiple developmental stressors. We modeled early life adversity in rats via maternal separation (postnatal day (P)2-20) and juvenile social isolation (P21-35). Adult (P85) male and female rats were assessed for differences in the presence and structural integrity of PFC perineuronal nets (PNNs) enwrapping parvalbumin (PV)-expressing interneurons. PNNs are extracellular matrix structures formed during critical periods in postnatal development that play a key role in the plasticity of PV cells. Females – but not males – exposed to multiple hits of adversity demonstrated a reduction in PFC PV cells in adulthood. We also observed a sex-specific, potentiated reduction in PV+ PNN structural integrity. Moreover, correlations between neural disruption and hyperactivity/risk-assessment behavior were altered by adversity differently in males and females. These findings suggest a sex-specific impact of repeated adversity on neurostructural development and implicate PNNs as a contributor to associated behavioral dysfunction.

Competing Interest Statement

The authors have declared no competing interest.

  • Abbreviations

    PFC
    prefrontal cortex
    PL
    prelimbic
    IL
    infralimbic
    PNN
    perineuronal net
    WFA
    Wisteria floribunda agglutinin
    MS
    maternal separation
    Con
    control
    SI
    social isolation
    PH
    pair-housed
    P
    postnatal day
    PBS
    phosphate buffered saline
    PFA
    paraformaldehyde
    EZM
    elevated zero maze
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    Posted October 25, 2020.
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    A two-hit adversity model in developing rats reveals sex-specific impacts on prefrontal cortex structure and behavior
    Kelsea R. Gildawie, Lilly M. Ryll, Jessica C. Hexter, Shayna Peterzell, Alissa A. Valentine, Heather C. Brenhouse
    bioRxiv 2020.10.23.352161; doi: https://doi.org/10.1101/2020.10.23.352161
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    A two-hit adversity model in developing rats reveals sex-specific impacts on prefrontal cortex structure and behavior
    Kelsea R. Gildawie, Lilly M. Ryll, Jessica C. Hexter, Shayna Peterzell, Alissa A. Valentine, Heather C. Brenhouse
    bioRxiv 2020.10.23.352161; doi: https://doi.org/10.1101/2020.10.23.352161

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