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

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.

[1]  M. Joëls,et al.  Opposite effects of glucocorticoid receptor activation on hippocampal CA1 dendritic complexity in chronically stressed and handled animals , 2008, Hippocampus.

[2]  M. Joëls,et al.  LTP after Stress: Up or Down? , 2007, Neural plasticity.

[3]  Claudia Buss,et al.  Maternal Care Modulates the Relationship between Prenatal Risk and Hippocampal Volume in Women But Not in Men , 2007, The Journal of Neuroscience.

[4]  S. Yamawaki,et al.  Importance of early lighting conditions in maternal care by dam as well as anxiety and memory later in life of offspring , 2007, The European journal of neuroscience.

[5]  R. Hakvoort,et al.  Variations of maternal care alter offspring levels of behavioural defensiveness in adulthood: Evidence for a threshold model , 2007, Behavioural Brain Research.

[6]  J. Dunn,et al.  Household chaos--links with parenting and child behaviour. , 2006, Journal of child psychology and psychiatry, and allied disciplines.

[7]  K. Braun,et al.  Lack of paternal care affects synaptic development in the anterior cingulate cortex , 2006, Brain Research.

[8]  Jonathan R. Whitlock,et al.  Learning Induces Long-Term Potentiation in the Hippocampus , 2006, Science.

[9]  H. Anisman,et al.  Maternal programming of defensive responses through sustained effects on gene expression , 2006, Biological Psychology.

[10]  M. Joëls Corticosteroid effects in the brain: U-shape it. , 2006, Trends in pharmacological sciences.

[11]  Ger J. A. Ramakers,et al.  Improved Long-Term Potentiation and Memory in Young Tau-P301L Transgenic Mice before Onset of Hyperphosphorylation and Tauopathy , 2006, The Journal of Neuroscience.

[12]  M. Joëls,et al.  Timing is essential for rapid effects of corticosterone on synaptic potentiation in the mouse hippocampus. , 2006, Learning & memory.

[13]  M. Joëls,et al.  Glucocorticoid receptor activation selectively hampers N-methyl-d-aspartate receptor dependent hippocampal synaptic plasticity in vitro , 2005, Neuroscience.

[14]  I. Weaver,et al.  Reversal of Maternal Programming of Stress Responses in Adult Offspring through Methyl Supplementation: Altering Epigenetic Marking Later in Life , 2005, The Journal of Neuroscience.

[15]  Melly S. Oitzl,et al.  Age-Related Changes in Hypothalamic-Pituitary-Adrenal Axis Activity of Male C57BL/6J Mice , 2005, Neuroendocrinology.

[16]  M. Meaney,et al.  Maternal care as a model for experience-dependent chromatin plasticity? , 2005, Trends in Neurosciences.

[17]  T. Bredy,et al.  Peripubertal environmental enrichment reverses the effects of maternal care on hippocampal development and glutamate receptor subunit expression , 2004, The European journal of neuroscience.

[18]  I. Weaver,et al.  Epigenetic programming by maternal behavior , 2004, Nature Neuroscience.

[19]  K. Braun,et al.  Juvenile emotional experience alters synaptic composition in the rodent cortex, hippocampus, and lateral amygdala , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[20]  C. Sandi,et al.  Prior exposure to a single stress session facilitates subsequent contextual fear conditioning in rats Evidence for a role of corticosterone , 2003, Hormones and Behavior.

[21]  M. Meaney,et al.  Variations in Maternal Care Alter GABAA Receptor Subunit Expression in Brain Regions Associated with Fear , 2003, Neuropsychopharmacology.

[22]  A. Mar,et al.  Variations in maternal care in the rat as a mediating influence for the effects of environment on development , 2003, Physiology & Behavior.

[23]  T. Bredy,et al.  Partial reversal of the effect of maternal care on cognitive function through environmental enrichment , 2003, Neuroscience.

[24]  M. Joëls,et al.  Chronic unpredictable stress impairs long‐term potentiation in rat hippocampal CA1 area and dentate gyrus in vitro , 2003, The European journal of neuroscience.

[25]  M. Joëls,et al.  Corticosterone and stress reduce synaptic potentiation in mouse hippocampal slices with mild stimulation , 2002, Neuroscience.

[26]  Eric Vermetten,et al.  Childhood trauma associated with smaller hippocampal volume in women with major depression. , 2002, The American journal of psychiatry.

[27]  K. Kendler,et al.  Toward a comprehensive developmental model for major depression in women. , 2002, The American journal of psychiatry.

[28]  E. R. Kloet,et al.  Reversal of cognitive deficit of apolipoprotein E knockout mice after repeated exposure to a common environmental experience , 2001, Neuroscience.

[29]  K. Braun,et al.  Juvenile emotional experience alters synaptic inputs on pyramidal neurons in the anterior cingulate cortex. , 2001, Cerebral cortex.

[30]  M. Joëls,et al.  Corticosteroid actions in hippocampus require DNA binding of glucocorticoid receptor homodimers , 2000, Nature Neuroscience.

[31]  J. Day,et al.  Maternal care, hippocampal synaptogenesis and cognitive development in rats , 2000, Nature Neuroscience.

[32]  S. Southwick,et al.  Decreased benzodiazepine receptor binding in prefrontal cortex in combat-related posttraumatic stress disorder. , 2000, The American journal of psychiatry.

[33]  M. Meaney,et al.  Nongenomic transmission across generations of maternal behavior and stress responses in the rat. , 1999, Science.

[34]  C. Sandi,et al.  Correlational relationship between shock intensity and corticosterone secretion on the establishment and subsequent expression of contextual fear conditioning. , 1998, Behavioral neuroscience.

[35]  Robert Nitsch,et al.  Morphological features of the entorhinal–hippocampal connection , 1998, Progress in Neurobiology.

[36]  M. Joëls,et al.  Brain corticosteroid receptor balance in health and disease. , 1998, Endocrine reviews.

[37]  Shakti Sharma,et al.  Maternal care during infancy regulates the development of neural systems mediating the expression of fearfulness in the rat. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[38]  Shakti Sharma,et al.  Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. , 1997, Science.

[39]  J. W. Rudy,et al.  A selective role for corticosterone in contextual-fear conditioning. , 1997, Behavioral neuroscience.

[40]  E. Kandel,et al.  Control of Memory Formation Through Regulated Expression of a CaMKII Transgene , 1996, Science.

[41]  S. Ogawa,et al.  Role of adrenal steroid mineralocorticoid and glucocorticoid receptors in long-term potentiation in the CA1 field of hippocampal slices , 1996, Brain Research.

[42]  J. Csernansky,et al.  Hippocampal atrophy in recurrent major depression. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[43]  P. Joyce,et al.  Disruptions in Childhood Parental Care as Risk Factors for Major Depression in Adult Women , 1995, The Australian and New Zealand journal of psychiatry.

[44]  R. F. Westbrook,et al.  Effects of the Interval between Exposure to a Novel Environment and the Occurrence of Shock on the Freezing Responses of Rats , 1994, The Quarterly journal of experimental psychology. B, Comparative and physiological psychology.

[45]  R. F. Westbrook,et al.  Effects of Exposure to a To-Be-Shocked Environment upon the Rat's Freezing Response: Evidence for Facilitation, Latent Inhibition, and Perceptual Learning , 1993, The Quarterly journal of experimental psychology. B, Comparative and physiological psychology.

[46]  D. Diamond,et al.  Inverted‐U relationship between the level of peripheral corticosterone and the magnitude of hippocampal primed burst potentiation , 1992, Hippocampus.

[47]  Joseph E LeDoux,et al.  Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. , 1992, Behavioral neuroscience.

[48]  L. Nadel,et al.  Early handling increases hippocampal long-term potentiation in young rats , 1986, Behavioural Brain Research.

[49]  T. Yamamoto,et al.  Postnatal ontogenesis of hippocampal CA1 area in rats. I. Development of dendritic arborisation in pyramidal neurons , 1981, Brain Research Bulletin.

[50]  D C Blanchard,et al.  Crouching as an index of fear. , 1969, Journal of comparative and physiological psychology.

[51]  M. Corner,et al.  Dynamics and plasticity in developing neuronal networks in vitro. , 2005, Progress in brain research.

[52]  C. Nemeroff Neurobiological consequences of childhood trauma. , 2004, The Journal of clinical psychiatry.

[53]  Charles B Nemeroff CB Early-Life Adversity, CRF Dysregulation, and Vulnerability to Mood and Anxiety Disorders. , 2004, Psychopharmacology bulletin.

[54]  N. Cb Early-Life Adversity, CRF Dysregulation, and Vulnerability to Mood and Anxiety Disorders. , 2004 .

[55]  B. McEwen Early life influences on life-long patterns of behavior and health. , 2003, Mental retardation and developmental disabilities research reviews.

[56]  A. Tang,et al.  Neonatal exposure to novelty enhances long‐term potentiation in CA1 of the rat hippocampus , 2002, Hippocampus.

[57]  M. Meaney,et al.  Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. , 2001, Annual review of neuroscience.

[58]  Stephen Maren Neurobiology of Pavlovian fear conditioning. , 2001, Annual review of neuroscience.

[59]  L. Staib,et al.  Hippocampal volume reduction in major depression. , 2000, The American journal of psychiatry.