Cited by 196Neuroscience and Neuropharmacology ResearchMemory and Neural MechanismsNeurogenesis and neuroplasticity mechanisms

The DOI matches its Crossref record; 59 of the 59 references it cites were found in a registry or an index.

Peripubertal environmental enrichment reverses the effects of maternal care on hippocampal development and glutamate receptor subunit expression

Bredy, Timothy W., Zhang, Tie Yuan, Grant, Rebecca J., Diorio, Josie, Meaney, Michael J.·2004·European Journal of Neuroscience

DOI 10.1111/j.1460-9568.2004.03599.x

Open this paper in CoChat — free account

Abstract

Maternal care in the rat influences the development of cognitive function in the offspring through neural systems known to mediate activity-dependent synaptic plasticity. The offspring of mothers that exhibit increased levels of pup licking/grooming (high-LG mothers) show increased hippocampal N-methyl-D-aspartate (NMDA) subunit mRNA expression, enhanced synaptogenesis and improved hippocampal-dependent spatial learning in comparison with animals reared by low-LG mothers. The effects of reduced maternal care on cognitive function are reversed with peripubertal environmental enrichment; however, the neural mechanisms mediating this effect are not known. In these studies we exposed the offspring of high- and low-LG mothers to environmental enrichment from days 22 to 70 of life, and measured the expression of genes encoding for glutamate receptor subunits and synaptophysin expression as a measure of synaptic density. Environmental enrichment reversed the effects of maternal care on synaptic density and this effect was, in turn, associated with a reversal of the effect of maternal care on the NR2A and NR2B subunits of the NMDA receptor, as well as effects on (RS)-alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptor subunits. Finally, direct infusion of an NR2B-specific NMDA receptor antagonist into the hippocampus eliminated the effects of maternal care on spatial learning/memory in the Morris water maze. These findings suggest that: (1) the effects of maternal care are mediated by changes in NR2B gene expression; and (2) that environmental enrichment reverses the effects of reduced maternal care through the same genomic target, the NR2B gene, and possibly effects on other subunits of the NMDA and AMPA receptors.

Integrity signals

Registry

Crossref · 10.1111/j.1460-9568.2004.03599.x

Cites

59 of 59 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding
Bradford, M. M. (1976) · Analytical Biochemistry · doi:10.1016/0003-2697(76)90527-3 · Cited by 255,302
More hippocampal neurons in adult mice living in an enriched environment
Kempermann, G., Kuhn, H. G., & Gage, F. H. (1997) · Nature · doi:10.1038/386493a0 · Cited by 3,586
Maternal Care, Hippocampal Glucocorticoid Receptors, and Hypothalamic-Pituitary-Adrenal Responses to Stress
Liu, D., Diorio, J., Tannenbaum, B., Caldji, C., Francis, D., Freedman, A., Sharma, S., Pearson, D., Plotsky, P. M., & Meaney, M. J. (1997) · Science · doi:10.1126/science.277.5332.1659 · Cited by 3,170
Self-citation
Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations
Meaney, M. J. (2001) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.24.1.1161 · Cited by 2,708
Self-citation
Heteromeric NMDA receptors: molecular and functional distinction of subtypes
Monyer, H., Sprengel, R., Schoepfer, R., Herb, A., Higuchi, M., Lomeli, H., Burnashev, N., Sakmann, B., & Seeburg, P. H. (1992) · Science · doi:10.1126/science.256.5060.1217 · Cited by 2,541
Neural consequences of enviromental enrichment
van Praag, H., Kempermann, G., & Gage, F. H. (2000) · Nature Reviews Neuroscience · doi:10.1038/35044558 · Cited by 2,468
The adaptive significance of maternal effects
Mousseau, T. A. (1998) · Trends in Ecology & Evolution · doi:10.1016/s0169-5347(98)01472-4 · Cited by 2,016
Nongenomic Transmission Across Generations of Maternal Behavior and Stress Responses in the Rat
Francis, D., Diorio, J., Liu, D., & Meaney, M. J. (1999) · Science · doi:10.1126/science.286.5442.1155 · Cited by 1,965
Self-citation
Genetic enhancement of learning and memory in mice
Tang, Y., Shimizu, E., Dubé, G., Rampon, C., Kerchner, G. A., Zhuo, M., Liu, G., & Tsien, J. Z. (1999) · Nature · doi:10.1038/43432 · Cited by 1,878
Maternal Effects As Adaptations
(1998) · doi:10.1093/oso/9780195111637.001.0001 · Cited by 1,653

Show all 59 references

Research works printed but not linked: 2

Hinde R.A., 1986, Development of Anti‐Social and Prosocial Behaviour, 13
O'Leary S.K., 2002, Persistence of environmental enrichment effects after prenatal alcohol exposure on Morris water maze performance, Dev. Psychobiol., 41, 318

Sorted by citations

Psychological well-being: evidence regarding its causes and consequences
Huppert, F. A. (2009) · Applied Psychology: Health and Well-Being · doi:10.1111/j.1758-0854.2009.01008.x · Cited by 1,583
Socioeconomic status and the brain: mechanistic insights from human and animal research
Hackman, D. A., Farah, M. J., & Meaney, M. J. (2010) · Nature Reviews Neuroscience · doi:10.1038/nrn2897 · Cited by 1,409
Self-citation
Epigenetics and the biological definition of gene×environment interactions
Meaney, M. J. (2010) · Child Development · doi:10.1111/j.1467-8624.2009.01381.x · Cited by 1,239
Self-citation
Stress effects on memory: An update and integration
Schwabe, L., Joëls, M., Roozendaal, B., Wolf, O. T., & Oitzl, M. S. (2012) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2011.07.002 · Cited by 714
Brain-Derived Neurotrophic Factor–5-HTTLPR Gene Interactions and Environmental Modifiers of Depression in Children
Kaufman, J., Yang, B.-Z., Douglas-Palumberi, H., Grasso, D., Lipschitz, D., Houshyar, S., Krystal, J. H., & Gelernter, J. (2006) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.10.026 · Cited by 692
Maternal care and hippocampal plasticity: evidence for experience-dependent structural plasticity, altered synaptic functioning, and differential responsiveness to glucocorticoids and stress
Champagne, D. L., Bagot, R. C., van Hasselt, F., Ramakers, G., Meaney, M. J., de Kloet, E. R., Joels, M., & Krugers, H. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.0526-08.2008 · Cited by 661
Neurobiological and psychiatric consequences of child abuse and neglect
Heim, C., Shugart, M., Craighead, W. E., & Nemeroff, C. B. (2010) · Developmental Psychobiology · doi:10.1002/dev.20494 · Cited by 613
Epigenetics and the environmental regulation of the genome and its function
Zhang, T.-Y., & Meaney, M. J. (2010) · Annual Review of Psychology · doi:10.1146/annurev.psych.60.110707.163625 · Cited by 565
Self-citation
Stress and the developing adolescent brain
Eiland, L. R., & Romeo, R. D. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.10.048 · Cited by 539
Abnormal brain connectivity in children after early severe socioemotional deprivation: A diffusion tensor imaging study
Eluvathingal, T. J., Chugani, H. T., Behen, M. E., Juhász, C., Muzik, O., Maqbool, M., Chugani, D. C., & Makki, M. (2006) · Pediatrics · doi:10.1542/peds.2005-1727 · Cited by 451
Broad Epigenetic Signature of Maternal Care in the Brain of Adult Rats
McGowan, P. O., Suderman, M., Sasaki, A., Huang, T. C. T., Hallett, M., Meaney, M. J., & Szyf, M. (2011) · PLoS ONE · doi:10.1371/journal.pone.0014739 · Cited by 452
Self-citation
The impact of environmental enrichment in laboratory rats—Behavioural and neurochemical aspects
Simpson, J., & Kelly, J. P. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.04.002 · Cited by 480
Aging, plasticity and environmental enrichment: Structural changes and neurotransmitter dynamics in several areas of the brain
Mora, F., Segovia, G., & Arco, A. D. (2007) · Brain Research Reviews · doi:10.1016/j.brainresrev.2007.03.011 · Cited by 431
Stress and the adolescent brain
ROMEO, R. D., & McEWEN, B. S. (2006) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1376.022 · Cited by 379
The programming of individual differences in defensive responses and reproductive strategies in the rat through variations in maternal care
Cameron, N. M., Champagne, F. A., Parent, C., Fish, E. W., Ozaki-Kuroda, K., & Meaney, M. J. (2005) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2005.03.022 · Cited by 320
Self-citation
Adolescence: A central event in shaping stress reactivity
Romeo, R. D. (2010) · Developmental Psychobiology · doi:10.1002/dev.20437 · Cited by 344
The Influence of Socioeconomic Status on Children’s Brain Structure
Jednoróg, K., Altarelli, I., Monzalvo, K., Fluss, J., Dubois, J., Billard, C., Dehaene‐Lambertz, G., & Ramus, F. (2012) · PLoS ONE · doi:10.1371/journal.pone.0042486 · Cited by 329
Age matters
McCutcheon, J. E., & Marinelli, M. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.06648.x · Cited by 299
Effects of chronic social stress in adolescence on anxiety and neuroendocrine response to mild stress in male and female rats
McCormick, C. M., Smith, C. L., & Mathews, I. Z. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.09.005 · Cited by 278
Investigations of HPA function and the enduring consequences of stressors in adolescence in animal models
McCormick, C. M., Mathews, I. Z., Thomas, C., & Waters, P. (2010) · Brain and Cognition · doi:10.1016/j.bandc.2009.06.003 · Cited by 276
Epigenetic influence of social experiences across the lifespan
Champagne, F. A. (2010) · Developmental Psychobiology · doi:10.1002/dev.20436 · Cited by 273
Influence of maternal care on the developing brain: Mechanisms, temporal dynamics and sensitive periods
Curley, J. P., & Champagne, F. A. (2015) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2015.11.001 · Cited by 279
Developmental plasticity of HPA and fear responses in rats: A critical review of the maternal mediation hypothesis
Macrı̀, S., & Würbel, H. (2006) · Hormones and Behavior · doi:10.1016/j.yhbeh.2006.06.015 · Cited by 258
Adolescent neurobiological susceptibility to social context
Schriber, R. A., & Guyer, A. E. (2016) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2015.12.009 · Cited by 246
The Neurobiological Toll of Child Abuse and Neglect
Neigh, G. N., Gillespie, C. F., & Nemeroff, C. B. (2009) · Trauma Violence & Abuse · doi:10.1177/1524838009339758 · Cited by 248
Review: Environmental enrichment and brain repair: harnessing the therapeutic effects of cognitive stimulation and physical activity to enhance experience‐dependent plasticity
Hannan, A. J. (2014) · Neuropathology and Applied Neurobiology · doi:10.1111/nan.12102 · Cited by 240
Stress during development: Impact on neuroplasticity and relevance to psychopathology
Fumagalli, F., Molteni, R., Racagni, G., & Riva, M. A. (2007) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2007.01.002 · Cited by 226
Maternal care determines rapid effects of stress mediators on synaptic plasticity in adult rat hippocampal dentate gyrus
Bagot, R. C., van Hasselt, F. N., Champagne, D. L., Meaney, M. J., Krugers, H. J., & Joëls, M. (2009) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2009.03.004 · Cited by 216
How social experiences influence the brain
Champagne, F. A., & Curley, J. P. (2005) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2005.10.001 · Cited by 225
Maternal programming of defensive responses through sustained effects on gene expression
Zhang, T.-Y., Bagot, R., Parent, C., Nesbitt, C., Bredy, T. W., Caldji, C., Fish, E., Anisman, H., Szyf, M., & Meaney, M. J. (2006) · Biological Psychology · doi:10.1016/j.biopsycho.2006.01.009 · Cited by 206
Clinical evaluation of multimodal environmental modification (MEMO) in the management of cats with idiopathic cystitis
Buffington, C. A. T., Westropp, J. L., Chew, D. J., & Bolus, R. R. (2006) · Journal of Feline Medicine and Surgery · doi:10.1016/j.jfms.2006.02.002 · Cited by 202
Social influences on neurobiology and behavior: Epigenetic effects during development
Curley, J. P., Jensen, C. L., Rahia Mashoodh, A., & Champagne, F. A. (2010) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2010.06.005 · Cited by 205
Environmental Change Enhances Cognitive Abilities in Fish
Kotrschal, A., & Taborsky, B. (2010) · PLoS Biology · doi:10.1371/journal.pbio.1000351 · Cited by 196
From the stressed adolescent to the anxious and depressed adult: Investigations in rodent models
McCormick, C. M., & Green, M. R. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.08.063 · Cited by 188
Maternal licking regulates hippocampal glucocorticoid receptor transcription through a thyroid hormone–serotonin–NGFI-A signalling cascade
Hellstrom, I. C., Dhir, S. K., Diorio, J. C., & Meaney, M. J. (2012) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2012.0223 · Cited by 171
The influence of natural variations in maternal care on play fighting in the rat
Parent, C. I., & Meaney, M. J. (2008) · Developmental Psychobiology · doi:10.1002/dev.20342 · Cited by 175
Self-citation
Developmental regulation of cognitive abilities: Modified composition of a molecular switch turns on associative learning
Dumas, T. C. (2005) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2005.08.002 · Cited by 182
Maternal care, isolation-induced infant ultrasonic calling, and their relations to adult anxiety-related behavior in the rat.
Wöhr, M., & Schwarting, R. K. W. (2008) · Behavioral Neuroscience · doi:10.1037/0735-7044.122.2.310 · Cited by 161
Reproductive experience differentially affects spatial reference and working memory performance in the mother
Pawluski, J. L., Walker, S. K., & Galea, L. A. M. (2005) · Hormones and Behavior · doi:10.1016/j.yhbeh.2005.05.016 · Cited by 154
Preventive Interventions for ADHD: A Neurodevelopmental Perspective
Halperin, J. M., Bedard, A., & Curchack, J. T. (2012) · Neurotherapeutics · doi:10.1007/s13311-012-0123-z · Cited by 151
Neurodevelopmental Optimization after Early-Life Adversity: Cross-Species Studies to Elucidate Sensitive Periods and Brain Mechanisms to Inform Early Intervention
Luby, J. L., Baram, T. Z., Rogers, C. E., & Barch, D. M. (2020) · Trends in Neurosciences · doi:10.1016/j.tins.2020.08.001 · Cited by 160
Environmental enrichment, prefrontal cortex, stress, and aging of the brain
Segovia, G., Arco, A. D., & Mora, F. (2009) · Journal of Neural Transmission · doi:10.1007/s00702-009-0214-0 · Cited by 140
Nonsteroidal Anti-Inflammatory Treatment Prevents Delayed Effects of Early Life Stress in Rats
Brenhouse, H. C., & Andersen, S. L. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.05.006 · Cited by 127
Early-life stress and cognitive outcome
Hedges, D. W., & Woon, F. L. M. (2010) · Psychopharmacology · doi:10.1007/s00213-010-2090-6 · Cited by 135
Shaping adult phenotypes through early life environments
Weaver, I. C. G. (2009) · Birth Defects Research Part C Embryo Today Reviews · doi:10.1002/bdrc.20164 · Cited by 121
Repeated maternal separation of male Wistar rats alters glutamate receptor expression in the hippocampus but not the prefrontal cortex
Pickering, C., Gustafsson, L., Cebere, A., Nylander, I., & Liljequist, S. (2006) · Brain Research · doi:10.1016/j.brainres.2006.04.136 · Cited by 115
Variations in postnatal maternal care and the epigenetic regulation of metabotropic glutamate receptor 1 expression and hippocampal function in the rat
Bagot, R. C., Zhang, T.-Y., Wen, X., Nguyen, T. T. T., Nguyen, H.-B., Diorio, J., Wong, T. P., & Meaney, M. J. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1204599109 · Cited by 141
Adult hippocampal glucocorticoid receptor expression and dentate synaptic plasticity correlate with maternal care received by individuals early in life
van Hasselt, F. N., Cornelisse, S., Yuan Zhang, T., Meaney, M. J., Velzing, E. H., Krugers, H. J., & Joëls, M. (2012) · Hippocampus · doi:10.1002/hipo.20892 · Cited by 109
Early Adversity and Developmental Outcomes: Interaction Between Genetics, Epigenetics, and Social Experiences Across the Life Span
Champagne, F. A. (2010) · Perspectives on Psychological Science · doi:10.1177/1745691610383494 · Cited by 110
Glutamate–dopamine–GABA interactions in the aging basal ganglia
Mora, F., Segovia, G., & Arco, A. D. (2007) · Brain Research Reviews · doi:10.1016/j.brainresrev.2007.10.006 · Cited by 118
Early life stress in epilepsy: A seizure precipitant and risk factor for epileptogenesis
van Campen, J. S., Jansen, F. E., Graan, P. N. E. D., Braun, K. P. J., & Joëls, M. (2013) · Epilepsy & Behavior · doi:10.1016/j.yebeh.2013.09.029 · Cited by 105
Length of Time Between Onset of Childhood Sexual Abuse and Emergence of Depression in a Young Adult Sample: A Retrospective Clinical Report
Teicher, M. H., Samson, J. A., Polcari, A., & Andersen, S. L. (2009) · The Journal of Clinical Psychiatry · doi:10.4088/jcp.08m04235 · Cited by 100
Neurobiological effects of neonatal maternal separation and post-weaning environmental enrichment.
Vivinetto, A. L., Suárez, M. M., & Rivarola, M. A. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.11.014 · Cited by 103
The association of child abuse and neglect with adult disability in schizophrenia and the prominent role of physical neglect
Gil, A., Gama, C. S., de Jesus, D. R., Lobato, M. I. R., Zimmer, M., & Belmonte-de-Abreu, P. S. (2009) · Child Abuse & Neglect · doi:10.1016/j.chiabu.2009.02.006 · Cited by 93
Late postnatal maturation of excitatory synaptic transmission permits adult-like expression of hippocampal-dependent behaviors
Dumas, T. C. (2005) · Hippocampus · doi:10.1002/hipo.20077 · Cited by 94
Maternal Programming of Defensive Responses Through Sustained Effects on Gene Expression
Meaney, M. J. (2007) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780195306255.003.0007 · Cited by 92
Within-litter variation in maternal care received by individual pups correlates with adolescent social play behavior in male rats.
van Hasselt, F. N., Tieskens, J. M., Trezza, V., Krugers, H. J., Vanderschuren, L. J. M. J., & Joëls, M. (2012) · Physiology & Behavior · doi:10.1016/j.physbeh.2011.12.007 · Cited by 91
Prenatal restraint stress and motherless rearing disrupts expression of plasticity markers and stress-induced corticosterone release in adult female Sprague–Dawley rats
Burton, C. L., Chatterjee, D., Chatterjee‐Chakraborty, M., Lovic, V., Grella, S. L., Steiner, M. S., & Fleming, A. S. (2007) · Brain Research · doi:10.1016/j.brainres.2007.05.003 · Cited by 91
Allostasis and the developing human brain: Explicit consideration of implicit models
Ganzel, B. L., & Morris, P. (2011) · Development and Psychopathology · doi:10.1017/s0954579411000447 · Cited by 93
Single, intense prenatal stress decreases emotionality and enhances learning performance in the adolescent rat offspring: Interaction with a brief, daily maternal separation
Cannizzaro, C., Plescia, F., Martire, M., Gagliano, M., Cannizzaro, G., Mantia, G., & Cannizzaro, E. (2006) · Behavioural Brain Research · doi:10.1016/j.bbr.2005.12.010 · Cited by 85
Effects of stressors in adolescence on learning and memory in rodent models
Green, M. R., & McCormick, C. M. (2013) · Hormones and Behavior · doi:10.1016/j.yhbeh.2012.09.012 · Cited by 86
Sensitive Periods in Epigenetics: Bringing us Closer to Complex Behavioral Phenotypes
Nagy, C., & Turecki, G. (2012) · Epigenomics · doi:10.2217/epi.12.37 · Cited by 81
Blockade of corticotropin‐releasing hormone receptor 1 attenuates early‐life stress‐induced synaptic abnormalities in the neonatal hippocampus
Liao, X., Yang, X., Jia, J., Li, J., Xie, X., Su, Y., Schmidt, M. V., Si, T., & Wang, X. (2014) · Hippocampus · doi:10.1002/hipo.22254 · Cited by 78
Adaptive significance of natural variations in maternal care in rats: A translational perspective
Beery, A. K., & Francis, D. D. (2011) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2011.03.012 · Cited by 81
Effects of early adolescent environmental enrichment on cognitive dysfunction, prefrontal cortex development, and inflammatory cytokines after early life stress
do Prado, C. H., Narahari, T., Holland, F. H., Lee, H., Murthy, S. K., & Brenhouse, H. C. (2015) · Developmental Psychobiology · doi:10.1002/dev.21390 · Cited by 75
Early Parental Deprivation in the Marmoset Monkey Produces Long-Term Changes in Hippocampal Expression of Genes Involved in Synaptic Plasticity and Implicated in Mood Disorder
Law, A. J., Pei, Q., Walker, M. A., Gordon-Andrews, H., Weickert, C. S., Feldon, J., Pryce, C. R., & Harrison, P. J. (2008) · Neuropsychopharmacology · doi:10.1038/npp.2008.106 · Cited by 74
Enriched environment ameliorates depression-induced cognitive deficits and restores abnormal hippocampal synaptic plasticity
Mahati, K., Bhagya, V. R., Christofer, T., Sneha, A., & Rao, B. S. S. (2016) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2016.08.017 · Cited by 80
Integrating Early Life Experience, Gene Expression, Brain Development, and Emergent Phenotypes
Weaver, I. C. G. (2014) · Advances in genetics · doi:10.1016/b978-0-12-800222-3.00011-5 · Cited by 74
Mutant mice with reduced NMDA-NR1 glycine affinity or lack of d-amino acid oxidase function exhibit altered anxiety-like behaviors
Labrie, V., Clapcote, S. J., & Roder, J. (2008) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2008.09.016 · Cited by 73
Litter size affects emotionality in adult male rats
Dimitsantos, E., Escorihuela, R. M., Fuentes, S., Armario, A., & Nadal, R. A. (2007) · Physiology & Behavior · doi:10.1016/j.physbeh.2007.05.066 · Cited by 72
Importance of early lighting conditions in maternal care by dam as well as anxiety and memory later in life of offspring
Toki, S., Morinobu, S., Imanaka, A., Yamamoto, S., Yamawaki, S., & Honma, K. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05288.x · Cited by 69
Maternal Care Influences Hippocampal N-Methyl-D-Aspartate Receptor Function and Dynamic Regulation by Corticosterone in Adulthood
Bagot, R. C., Tse, Y. C., Nguyen, H.-B., Wong, A. S., Meaney, M. J., & Wong, T. P. (2012) · Biological Psychiatry · doi:10.1016/j.biopsych.2012.03.016 · Cited by 65
Self-citation
Epigenetic Manipulation of Brain-derived Neurotrophic Factor Improves Memory Deficiency Induced by Neonatal Anesthesia in Rats
Wu, J., Bie, B., & Naguib, M. (2015) · Anesthesiology · doi:10.1097/aln.0000000000000981 · Cited by 65
Resilience priming: Translational models for understanding resiliency and adaptation to early life adversity
Kentner, A. C., Cryan, J. F., & Brummelte, S. (2019) · Developmental Psychobiology · doi:10.1002/dev.21775 · Cited by 64
Early environments, glucocorticoid receptors, and behavioral epigenetics.
Champagne, F. A. (2013) · Behavioral Neuroscience · doi:10.1037/a0034186 · Cited by 65
Stress and the Emerging Roles of Chromatin Remodeling in Signal Integration and Stable Transmission of Reversible Phenotypes
Weaver, I. C. G., Korgan, A. C., Lee, K., Wheeler, R. V., Hundert, A. S., & Goguen, D. (2017) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2017.00041 · Cited by 69
Anxiety-like behaviour in adult rats perinatally exposed to maternal calorie restriction
Levay, E. A., Paolini, A. G., Govic, A., Hazi, A., Penman, J., & Kent, S. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.03.021 · Cited by 62
Environmental enrichment mitigates the sex-specific effects of gestational inflammation on social engagement and the hypothalamic pituitary adrenal axis-feedback system
Connors, E. J., Shaik, A. N., Migliore, M. M., & Kentner, A. C. (2014) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2014.06.020 · Cited by 61
Epigenetic alterations associated with war trauma and childhood maltreatment
Ramo‐Fernández, L., Schneider, A., Wilker, S., & Kolassa, I. (2015) · Behavioral Sciences & the Law · doi:10.1002/bsl.2200 · Cited by 59
Epigenetics/Programming in the HPA Axis
Buschdorf, J. P., & Meaney, M. J. (2015) · Comprehensive physiology · doi:10.1002/cphy.c140027 · Cited by 64
NMDA neurotransmission as a critical mediator of borderline personality disorder
Grosjean, B., & Tsai, G. E. (2007) · Journal of Psychiatry and Neuroscience · doi:10.1139/jpn.0710 · Cited by 57
Is exposure to enriched environment beneficial for functional post-lesional recovery in temporal lobe epilepsy?
Dhanushkodi, A., & Shetty, A. K. (2007) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2007.10.004 · Cited by 56
Genetic, epigenetic and environmental impact on sex differences in social behavior
Shepard, K. N., Michopoulos, V., Toufexis, D. J., & Wilson, M. E. (2009) · Physiology & Behavior · doi:10.1016/j.physbeh.2009.02.016 · Cited by 61
Correction: The Influence of Socioeconomic Status on Children’s Brain Structure
Jednoróg, K., Altarelli, I., Monzalvo, K., Fluss, J., Dubois, J., Billard, C., Dehaene‐Lambertz, G., & Ramus, F. (2012) · PLoS ONE · doi:10.1371/annotation/47661de2-2c53-4396-9f88-06b5ad233566 · Cited by 57
Environmental enrichment: Evidence for an unexpected therapeutic influence
Kotloski, R. J., & Sutula, T. P. (2014) · Experimental Neurology · doi:10.1016/j.expneurol.2014.11.012 · Cited by 54
Peer pressures: Social instability stress in adolescence and social deficits in adulthood in a rodent model
McCormick, C. M., Hodges, T. E., & Simone, J. J. (2014) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2014.04.002 · Cited by 56
Memory impairments and hippocampal modifications in adult rats with neonatal isolation stress experience
Kosten, T. A., Karanian, D. A., Yeh, J., Haile, C. N., Kim, J. J., Kehoe, P., & Bahr, B. A. (2007) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2007.03.011 · Cited by 51
New Frontiers in Animal Research of Psychiatric Illness
Kaffman, A., & Krystal, J. J. (2012) · Methods in Molecular Biology · doi:10.1007/978-1-61779-458-2_1 · Cited by 59
Increased expression of the NR2A NMDA receptor subunit in the prefrontal cortex of rats reared in isolation
Turnock-Jones, J. J., Jennings, C. A., Robbins, M. J., Cluderay, J. E., Cilia, J., Reid, J. L., Taylor, A. R., Jones, D. N. C., Emson, P. C., & Southam, E. (2009) · Synapse · doi:10.1002/syn.20665 · Cited by 49
Adolescent brain development: Current themes and future directions
Luciana, M. M. (2009) · Brain and Cognition · doi:10.1016/j.bandc.2009.11.002 · Cited by 54
Influence of environmental enrichment on steady-state mRNA levels for EAAC1, AMPA1 and NMDA2A receptor subunits in rat hippocampus
Andin, J., Hallbeck, M., Mohammed, A. H. S., & Marcusson, J. O. (2007) · Brain Research · doi:10.1016/j.brainres.2007.06.101 · Cited by 48
Maternal Care Differentially Affects Neuronal Excitability and Synaptic Plasticity in the Dorsal and Ventral Hippocampus
Nguyen, H., Bagot, R. C., Diorio, J. C., Wong, T. P., & Meaney, M. J. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.19 · Cited by 47
Early life modulators and predictors of adult synaptic plasticity
Akers, K. G., Nakazawa, M., Romeo, R. D., Connor, J. A., McEwen, B. S., & Tang, A. C. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.04921.x · Cited by 47
Neonatal paternal deprivation or early deprivation reduces adult parental behavior and central estrogen receptor α expression in mandarin voles (Microtus mandarinus)
Jia, R., Tai, F., An, S.-C., & Zhang, X. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.05.042 · Cited by 47
Hippocampal GluR1 associates with behavior in the elevated plus maze and shows sex differences
Xiang, X., Huang, W., Haile, C. N., & Kosten, T. A. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.03.068 · Cited by 45
Perinatal and juvenile social environments interact to shape cognitive behaviour and neural phenotype in prairie voles
Prounis, G. S., Foley, L., Rehman, A., & Ophir, A. G. (2015) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2015.2236 · Cited by 44
Effect of resource availability on biparental care, and offspring neural and behavioral development in the California mouse (Peromyscus californicus)
Bredy, T. W., Brown, R. E., & Meaney, M. J. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.05266.x · Cited by 44
Maternal care associates with play dominance rank among adult female rats
Parent, C. I., Corpo, A. D., Cameron, N. M., & Meaney, M. J. (2012) · Developmental Psychobiology · doi:10.1002/dev.21070 · Cited by 45
Pre-reproductive maternal enrichment influences rat maternal care and offspring developmental trajectories: behavioral performances and neuroplasticity correlates
Cutuli, D., Caporali, P., Gelfo, F., Angelucci, F., Laricchiuta, D., Foti, F., Bartolo, P. D., Bisicchia, E., Molinari, M., Vecchioli, S. F., et al. (2015) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2015.00066 · Cited by 43
Early handling effect on female rat spatial and non-spatial learning and memory
Plescia, F., Marino, R. A. M., Navarra, M., Gambino, G., Brancato, A., Sardo, P., & Cannizzaro, C. (2013) · Behavioural Processes · doi:10.1016/j.beproc.2013.10.011 · Cited by 42

Authors: Bredy, T. W., Zhang, T. Y., Grant, R. J., Diorio, J., & Meaney, M. J.
Affiliations: Douglas Mental Health University Institute (CA)
McGill University (CA)
Corresponding author: Meaney, Michael J.
ORCID: Bredy, Timothy W.
Meaney, Michael J.
Venue: European Journal of Neuroscience
Publisher: Wiley
Published: 2004-09
Volume: 20
Issue: 5
Pages: 1355-1362
ISSN: 0953-816X (ISSN-L)
1460-9568
DOI: 10.1111/j.1460-9568.2004.03599.x
OpenAlex: W2136757585
Cited by: 196
References: 59
Citations by year: 2026: 5 · 2024: 4 · 2023: 4 · 2022: 2 · 2021: 2 · 2020: 2 · 2019: 5 · 2018: 11 · 2017: 3 · 2016: 9 · 2015: 21 · 2014: 7 · 2013: 11 · 2012: 15
FWCI: 4.45
Type: journal article
Language: en
Open access: closed
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: European Journal of Neuroscience (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
Keywords: maternal care, environmental enrichment, hippocampus, NMDA receptor, NR2B subunit, AMPA receptors, glutamate receptor subunits, synaptophysin, synaptic density, spatial learning and memory, peripubertal period, synaptic plasticity, gene expression
MeSH terms: Age Factors, Animals, Environment, Female, Hippocampus, Male, Maternal Behavior, Receptors, Glutamate, Gene Expression Regulation, Developmental, Maze Learning, Rats, Long-Evans, Protein Subunits, Rats

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Peripubertal environmental enrichment reverses the effects of maternal care on hippocampal development and glutamate receptor subunit expression

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Citations

Cites

Cited by

Related

Metadata

Record

About these checks