Maternal care and hippocampal plasticity: Evidence for experience-dependent structural plasticity, altered synaptic functioning, and differential responsiveness to glucocorticoids and stress

Danielle L. Champagne*, Rosemary C. Bagot, Felisa van Hasselt, Ger Ramakers, Michael J. Meaney, E. Ronald de Kloet, Marian Joels, Harm Krugers

*Corresponding author for this work

Research output: Contribution to journalArticleAcademicpeer-review

529 Citations (Scopus)

Abstract

Maternal licking and grooming (LG) in infancy influences stress responsiveness and cognitive performance in the offspring. We examined the effects of variation in the frequency of pup LG on morphological, electrophysiological, and behavioral aspects of hippocampal synaptic plasticity under basal and stress-like conditions. We found shorter dendritic branch length and lower spine density in CA1 cells from the adult offspring of low compared with high LG offspring. We also observed dramatic effects on long-term potentiation (LTP) depending on corticosterone treatment. Low LG offspring, in contrast to those of high LG mothers, displayed significantly impaired LTP under basal conditions but surprisingly a significantly enhanced LTP in response to high corticosterone in vitro. This enhanced plasticity under conditions that mimic those of a stressful event was apparent in vivo. Adult low LG offspring displayed enhanced memory relative to high LG offspring when tested in a hippocampal-dependent, contextual fear-conditioning paradigm. Hippocampal levels of glucocorticoid and mineralocorticoid receptors were reduced in low compared with high LG offspring. Such effects, as well as the differences in dendritic morphology, likely contribute to LTP differences under resting conditions, as well as to the maternal effects on synaptic plasticity and behavior in response to elevated corticosterone levels. These results suggest that maternal effects may modulate optimal cognitive functioning in environments varying in demand in later life, with offspring of high and low LG mothers showing enhanced learning under contexts of low and high stress, respectively.

Original languageEnglish
Pages (from-to)6037-6045
Number of pages9
JournalThe Journal of Neuroscience
Volume28
Issue number23
DOIs
Publication statusPublished - 4-Jun-2008
Externally publishedYes

Keywords

  • CA1 hippocampus
  • corticosterone
  • long-term potentiation
  • maternal behavior
  • morphology
  • synaptic plasticity
  • LONG-TERM POTENTIATION
  • RECEPTOR SUBUNIT EXPRESSION
  • ANTERIOR CINGULATE CORTEX
  • MAJOR DEPRESSION
  • IN-VITRO
  • ENVIRONMENTAL ENRICHMENT
  • PYRAMIDAL NEURONS
  • GENE-EXPRESSION
  • CA1 AREA
  • FEAR

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