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Brain Structure and Function

, Volume 224, Issue 5, pp 1831–1843 | Cite as

Controllable stress elicits circuit-specific patterns of prefrontal plasticity in males, but not females

  • Michael V. Baratta
  • Tina M. Gruene
  • Samuel D. Dolzani
  • Lauren E. Chun
  • Steven F. Maier
  • Rebecca M. ShanskyEmail author
Original Article

Abstract

Actual or perceived behavioral control during a traumatic event can promote resilience against future adversity, but the long-term cellular and circuit mechanisms by which this protection is conferred have not been identified. Clinical outcomes following trauma exposure differ in men and women, and, therefore, it is especially important in preclinical research to dissect these processes in both males and females. In male adult rats, an experience with behavioral control over tail shock (“escapable stress”, ES) has been shown to block the neurochemical and behavioral outcomes produced by later uncontrollable tail shock (“inescapable stress”, IS), a phenomenon termed “behavioral immunization”. Here, we determined whether behavioral immunization is present in females. Unlike males, the stress-buffering effects of behavioral control were absent in female rats. We next examined the effects of ES and IS on spine morphology of dorsal raphe nucleus (DRN)–projecting prelimbic (PL) neurons, a circuit critical to the immunizing effects of ES in males. In males, IS elicited broad, non-specific alterations in PL spine size, while ES elicited PL–DRN circuit-specific spine changes. In contrast, females exhibited broad, non-specific spine enlargement after ES but only minor alterations after IS. These data provide evidence for a circuit-specific mechanism of structural plasticity that could underlie sexual divergence in the protective effects of behavioral control.

Keywords

Coping Medial prefrontal cortex Dorsal raphe nucleus Dendritic spines Structural plasticity Learned helplessness 

Notes

Acknowledgements

This work was supported by NIH Grants R01 MH050479 (SFM), R21 MH106817 (MVB), T32 MH016880 (SDD), a NARSAD Young Investigator Grant from the Brain and Behavior Research Foundation (MVB), and a Dissertation Research Grant from Northeastern University (TMG). The authors thank Alexis Stefano for spine illustrations (Figs. 1 and 6) and Nathan Leslie and Isabella Fallon for technical assistance.

Compliance with ethical standards

Conflict of Interest

The authors declare no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted.

Supplementary material

429_2019_1875_MOESM1_ESM.docx (2.9 mb)
Supplementary material 1 (docx 2937 kb)

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Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Michael V. Baratta
    • 1
  • Tina M. Gruene
    • 2
  • Samuel D. Dolzani
    • 1
  • Lauren E. Chun
    • 1
  • Steven F. Maier
    • 1
  • Rebecca M. Shansky
    • 2
    Email author
  1. 1.Department of Psychology and NeuroscienceUniversity of Colorado BoulderBoulderUSA
  2. 2.Department of PsychologyNortheastern UniversityBostonUSA

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