Rapid effects of estradiol and its receptor agonists on object recognition and object placement in adult male zebrafish

Behav Brain Res. 2020 Apr 20:384:112514. doi: 10.1016/j.bbr.2020.112514. Epub 2020 Jan 28.

Abstract

In recent years, there has been a growing appreciation that 17β-estradiol (E2) can rapidly modulate learning and memory processes by binding to membrane estrogen receptors and cause the activation of a number of signaling cascades within the central nervous system. In this study, we sought to investigate the effects of post-training administration of E2 (100 ng/g, 1 μg/g, 10 μg/g) and involvement of the estrogen receptors (ERs) using selective ER agonists on the consolidation of object recognition (OR) and object placement memory (OP) in adult male zebrafish. The general activation of ERs with the highest E2 dose improved consolidation of memory in both learning tasks within 1.45 h of administration. Activation of classical ERs (ERα and ERβ) improved consolidation of OR memory, but had no effect on fish performance in OP task. On the other hand, activation of G protein-coupled ER1 impaired and enhanced consolidation of OR and OP memories, respectively. Memory improvement in both tasks was accompanied by a marked up-regulation in the expression of genes encoding ionotropic and metabotropic glutamate receptors in a task-dependent manner. In contrast, the down-regulation in the expression of certain ionotropic glutamate receptors was observed in fish with impaired OR memory. Moreover, our study also revealed an increase in the transcript abundance of genes associated with synaptic protein synthesis (brain-derived neurotrophic factor, synaptophysin, and the mechanistic target of rapamycin). These results suggest that E2 may affect consolidation of memory in zebrafish likely through rapid changes in synaptic morphology and function.

Keywords: Estrogens; Object placement; Object recognition; Zebrafish.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Brain / drug effects*
  • Brain / metabolism
  • Brain-Derived Neurotrophic Factor / genetics
  • Cyclopentanes / pharmacology
  • Estradiol / pharmacology*
  • Estrogen Receptor alpha / agonists
  • Estrogen Receptor beta / agonists
  • Estrogens / pharmacology*
  • Learning / drug effects
  • Learning / physiology
  • Male
  • Memory Consolidation / drug effects*
  • Memory Consolidation / physiology
  • Nitriles / pharmacology
  • Phenols / pharmacology
  • Pyrazoles / pharmacology
  • Quinolines / pharmacology
  • RNA, Messenger / metabolism
  • Receptors, AMPA / genetics
  • Receptors, Metabotropic Glutamate / genetics
  • Receptors, N-Methyl-D-Aspartate / genetics
  • Recognition, Psychology / drug effects*
  • Recognition, Psychology / physiology
  • Reverse Transcriptase Polymerase Chain Reaction
  • Spatial Memory / drug effects*
  • Spatial Memory / physiology
  • Synaptophysin / genetics
  • TOR Serine-Threonine Kinases / genetics
  • Zebrafish
  • Zebrafish Proteins / agonists

Substances

  • 1-(4-(6-bromobenzo(1,3)dioxol-5-yl)-3a,4,5,9b-tetrahydro-3H-cyclopenta(c)quinolin-8-yl)ethanone
  • 2,3-bis(4-hydroxyphenyl)-propionitrile
  • Brain-Derived Neurotrophic Factor
  • Cyclopentanes
  • Estrogen Receptor alpha
  • Estrogen Receptor beta
  • Estrogens
  • Nitriles
  • Phenols
  • Pyrazoles
  • Quinolines
  • RNA, Messenger
  • Receptors, AMPA
  • Receptors, Metabotropic Glutamate
  • Receptors, N-Methyl-D-Aspartate
  • Synaptophysin
  • Zebrafish Proteins
  • metabotropic glutamate receptor type 1
  • 4,4',4''-(4-propyl-((1)H)-pyrazole-1,3,5-triyl) tris-phenol
  • Estradiol
  • TOR Serine-Threonine Kinases