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The Journal of Neuroscience, June 4, 2008, 28(23):6037-6045; doi:10.1523/JNEUROSCI.0526-08.2008

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Behavioral/Systems/Cognitive
Maternal Care and Hippocampal Plasticity: Evidence for Experience-Dependent Structural Plasticity, Altered Synaptic Functioning, and Differential Responsiveness to Glucocorticoids and Stress

Danielle L. Champagne,^1,3 Rosemary C. Bagot,⁴ Felisa van Hasselt,¹ Ger Ramakers,² Michael J. Meaney,⁴ E. Ronald de Kloet,³ Marian Joëls,¹ and Harm Krugers¹

¹Swammerdam Institute for Life Sciences Center for Neuroscience and ²Netherlands Institute for Neurosciences, University of Amsterdam, 1098 SM Amsterdam, The Netherlands, ³Leiden/Amsterdam Center for Drug Research, Leiden University Medical Centre, 2300 RA Leiden, The Netherlands, and ⁴Douglas Mental Health University Institute, McGill University, Montreal, Quebec, Canada H4H 1R3

Correspondence should be addressed to Danielle L. Champagne, Department of Medical Pharmacology, Leiden/Amsterdam Center for Drug Research, Leiden University Medical Centre, Gorlaeus Laboratoria, Einsteinweg 55, P.O. Box 9502, 2300 RA Leiden, The Netherlands. Email: d.champagne{at}chem.leidenuniv.nl

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.

Key words: CA1 hippocampus; corticosterone; long-term potentiation; maternal behavior; morphology; synaptic plasticity

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Received Oct. 10, 2007; revised April 7, 2008; accepted April 24, 2008.

Correspondence should be addressed to Danielle L. Champagne, Department of Medical Pharmacology, Leiden/Amsterdam Center for Drug Research, Leiden University Medical Centre, Gorlaeus Laboratoria, Einsteinweg 55, P.O. Box 9502, 2300 RA Leiden, The Netherlands. Email: d.champagne{at}chem.leidenuniv.nl

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