Stress differentially alters mu opioid receptor density and trafficking in parvalbumin-containing interneurons in the female and male rat hippocampus

Teresa A. Milner, Suzanne R. Burstein, Gina F. Marrone, Sana Khalid, Andreina D. Gonzalez, Tanya J. Williams, Kathryn C. Schierberl, Annelyn Torres-Reveron, Keith L. Gonzales, Bruce S. Mcewen, Elizabeth M. Waters

Research output: Contribution to journalArticlepeer-review

Abstract

Stress differentially affects hippocampal-dependent learning relevant to addiction and morphology in male and female rats. Mu opioid receptors (MORs), which are located in parvalbumin (PARV)-containing GABAergic interneurons and are trafficked in response to changes in the hormonal environment, play a critical role in promoting principal cell excitability and long-term potentiation. Here, we compared the effects of acute and chronic immobilization stress (AIS and CIS) on MOR trafficking in PARV-containing neurons in the hilus of the dentate gyrus in female and male rats using dual label immunoelectron microscopy. Following AIS, the density of MOR silver-intensified gold particles (SIGs) in the cytoplasm of PARV-labeled dendrites was significantly reduced in females (estrus stage). Conversely, AIS significantly increased the proportion of cytoplasmic MOR SIGs in PARV-labeled dendrites in male rats. CIS significantly reduced the number of PARV-labeled neurons in the dentate hilus of males but not females. However, MOR/PARV-labeled dendrites and terminals were significantly smaller in CIS females, but not males, compared with controls. Following CIS, the density of cytoplasmic MOR SIGs increased in PARV-labeled dendrites and terminals in females. Moreover, the proportion of near-plasmalemmal MOR SIGs relative to total decreased in large PARV-labeled dendrites in females. After CIS, no changes in the density or trafficking of MOR SIGs were seen in PARV-labeled dendrites or terminals in males. These data show that AIS and CIS differentially affect available MOR pools in PARV-containing interneurons in female and male rats. Furthermore, they suggest that CIS could affect principal cell excitability in a manner that maintains learning processes in females but not males.

Original languageEnglish (US)
Pages (from-to)757-772
Number of pages16
JournalSynapse
Volume67
Issue number11
DOIs
StatePublished - Nov 2013
Externally publishedYes

Keywords

  • Acute stress
  • Chronic stress
  • Estrogens
  • Opioids
  • Sex differences

ASJC Scopus subject areas

  • Cellular and Molecular Neuroscience

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