Insensitivity of the hippocampus to environmental stimulation during postnatal development

Waters, Nicholas S.; Klintsova, Anna Y.; Foster, Thomas C.

doi:10.1523/jneurosci.17-20-07967.1997

Cited by 46Memory and Neural MechanismsNeurogenesis and neuroplasticity mechanismsNeuroscience and Neuropharmacology Research

Insensitivity of the hippocampus to environmental stimulation during postnatal development

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Waters, Nicholas S., Klintsova, Anna Y., Foster, Thomas C.·1997·The Journal of Neuroscience

DOI 10.1523/jneurosci.17-20-07967.1997PMC PMC6793919

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Abstract

Development of cortical sensory systems is influenced by environmental experience during "sensitive periods," before onset of behavioral function. During these periods, synaptic plasticity is observed, and neuronal function shows increased responsiveness to environmental stimulation. Because the hippocampus is late to develop, and because it demonstrates synaptic plasticity before the onset of behavioral function, this experiment was designed to determine whether, like the sensory cortices, the hippocampus undergoes a period of enhanced responsiveness to the environment. Rats at three ages [postnatal day 16 (P16), P23, and P30] were tested on a hippocampally dependent task, spontaneous alternation, and exposed to a novel environment. They were then killed and processed for immunocytochemistry to Fos or for in vitro electrophysiology in hippocampal area CA1. Age-matched control subjects were killed immediately after removal from the home cage. Spontaneous alternation was only observed in the oldest (P30) animals. In these same animals, the environmental manipulation resulted in an increase in Fos-like immunoreactivity (FL-IR), relative to controls, and a decrease in the ability to induce long-term potentiation (LTP). In P16 and P23 animals, the environmental manipulation resulted in no differences in hippocampal FL-IR or LTP. These results suggest that, rather than showing increased responsiveness to the environment at these ages, the hippocampus is environmentally insensitive and that it is isolated from the effects of environmental stimuli. The hippocampus, a neural region important for higher cognitive function, may develop via a mechanism different from those observed in the primary sensory cortices.

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Morgan, J., & Curran, T. (1991) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.14.030191.002225 · Cited by 2,689 · see citing works
The regulation and function of c-fos and other immediate early genes in the nervous system
Sheng, M., & Greenberg, M. E. (1990) · Neuron · doi:10.1016/0896-6273(90)90106-p · Cited by 2,432 · see citing works
Developmental mechanisms that generate precise patterns of neuronal connectivity
Goodman, C. S., & Shatz, C. J. (1993) · Cell · doi:10.1016/s0092-8674(05)80030-3 · Cited by 1,425 · see citing works
The use of c-fos as a metabolic marker in neuronal pathway tracing
Dragunow, M., & Faull, R. (1989) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(89)90150-7 · Cited by 1,416 · see citing works
Maturation of the adrenocortical stress response: Neuroendocrine control mechanisms and the stress hyporesponsive period
Sapolsky, R. M., & Meaney, M. J. (1986) · Brain Research Reviews · doi:10.1016/0165-0173(86)90010-x · Cited by 991 · see citing works
Development of the hippocampal region in the rat I. Neurogenesis examined with 3 H‐thymidine autoradiography
Bayer, S. A. (1980) · The Journal of Comparative Neurology · doi:10.1002/cne.901900107 · Cited by 913 · see citing works
Blockade of "NMDA" Receptors Disrupts Experience-Dependent Plasticity of Kitten Striate Cortex
Kleinschmidt, A. K., Bear, M. F., & Singer, W. (1987) · Science · doi:10.1126/science.2443978 · Cited by 906 · see citing works
Deciphering The Hippocampal Polyglot: the Hippocampus as a Path Integration System
McNaughton, B. L., Barnes, C. A., Gerrard, J. L., Gothard, K. M., Jung, M. W., Knierim, J. J., Kudrimoti, H. S., Qin, Y., Skaggs, W. E., Suster, M. S., et al. (1996) · Journal of Experimental Biology · doi:10.1242/jeb.199.1.173 · Cited by 900 · see citing works
Impulse activity and the patterning of connections during cns development
Shatz, C. J. (1990) · Neuron · doi:10.1016/0896-6273(90)90333-b · Cited by 766 · see citing works
A critical period for long-term potentiation at thalamocortical synapses
Crair, M. C., & Malenka, R. C. (1995) · Nature · doi:10.1038/375325a0 · Cited by 691 · see citing works
Experience-dependent modification of synaptic plasticity in visual cortex
Kirkwood, A., Rioult, M., & Bear, M. (1996) · Nature · doi:10.1038/381526a0 · Cited by 666 · see citing works
Development of the mossy fibers of the dentate gyrus: I. A light and electron microscopic study of the mossy fibers and their expansions
Amaral, D. G., & Dent, J. A. (1981) · The Journal of Comparative Neurology · doi:10.1002/cne.901950106 · Cited by 606 · see citing works
Disruption of experience-dependent synaptic modifications in striate cortex by infusion of an NMDA receptor antagonist
Bear, M., Kleinschmidt, A., Gu, Q., & Singer, W. (1990) · The Journal of Neuroscience · doi:10.1523/jneurosci.10-03-00909.1990 · Cited by 488 · see citing works
Inescapable versus escapable shock modulates long-term potentiation in the rat hippocampus
Shors, T. J., Seib, T. B., Levine, S., & Thompson, R. F. (1989) · Science · doi:10.1126/science.2704997 · Cited by 458 · see citing works
NMDA receptors in the visual cortex of young kittens are more effective than those of adult cats
Tsumoto, T., Hagihara, K., Sato, H., & Hata, Y. (1987) · Nature · doi:10.1038/327513a0 · Cited by 440 · see citing works
Behavioral stress impairs long-term potentiation in rodent hippocampus
Foy, M. R., Stanton, M. E., Levine, S., & Thompson, R. F. (1987) · Behavioral and Neural Biology · doi:10.1016/s0163-1047(87)90664-9 · Cited by 436 · see citing works
Behavioral stress modifies hippocampal plasticity through N-methyl-D-aspartate receptor activation.
Kim, J. J., Foy, M. R., & Thompson, R. F. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.10.4750 · Cited by 435 · see citing works
Co-regulation of long-term potentiation and experience-dependent synaptic plasticity in visual cortex by age and experience
Kirkwood, A., Lee, H., & Bear, M. F. (1995) · Nature · doi:10.1038/375328a0 · Cited by 424 · see citing works
A simple perfusion chamber for the study of nervous tissue slices in vitro
Haas, H. L., Schaerer, B., & Vosmansky, M. (1979) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(79)90021-9 · Cited by 374 · see citing works
Induction and habituation of immediate early gene expression in rat brain by acute and repeated restraint stress
Melia, K. R., Ryabinin, A. E., Schroeder, R., Bloom, F. E., & Wilson, M. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-10-05929.1994 · Cited by 359 · see citing works
A quantitative electron microscopic study of synaptogenesis in the dentate gyrus of the rat
Crain, B. J., Cotman, C. W., Taylor, D. A., & LYNCH, G. S. (1973) · Brain Research · doi:10.1016/0006-8993(73)90088-7 · Cited by 349 · see citing works
Emergence of order in visual system development.
Shatz, C. J. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.2.602 · Cited by 349 · see citing works
Spatial Selectivity of Rat Hippocampal Neurons: Dependence on Preparedness for Movement
Foster, T. C., Castro, C. A., & McNaughton, B. L. (1989) · Science · doi:10.1126/science.2740902 · Cited by 323 · see citing works
NMDA receptor antagonists disrupt the retinotectal topographic map
Cline, H. T., & Constantine‐Paton, M. (1989) · Neuron · doi:10.1016/0896-6273(89)90201-8 · Cited by 285 · see citing works
The Pituitary-Adrenocortical System of Neonatal Rats Is Responsive to Stress throughout Development in a Time-Dependent and Stressor-Specific Fashion*
Walker, C., Scribner, K. A., Cascio, C. S., & Dallman, M. F. (1991) · Endocrinology · doi:10.1210/endo-128-3-1385 · Cited by 255 · see citing works
The Development of Hippocampal Function: Implications for Theory and for Therapy
Douglas, R. J. (1975) · Springer eBooks · doi:10.1007/978-1-4684-2979-4_11 · Cited by 254 · see citing works
Developmental onset of long‐term potentiation in area CA1 of the rat hippocampus.
Harris, K. M., & Teyler, T. J. (1984) · The Journal of Physiology · doi:10.1113/jphysiol.1984.sp015005 · Cited by 252 · see citing works
Ontogeny of contextual fear conditioning in rats: Implications for consolidation, infantile amnesia, and hippocampal system function.
Rudy, J. W., & Morledge, P. (1994) · Behavioral Neuroscience · doi:10.1037//0735-7044.108.2.227 · Cited by 245 · see citing works
Neuronal activity in the hippocampus during delayed non‐match to sample performance in rats: Evidence for hippocampal processing in recognition memory
Otto, T., & Eichenbaum, H. (1992) · Hippocampus · doi:10.1002/hipo.450020310 · Cited by 232 · see citing works
Ontogeny of spatial navigation behaviors in the rat: Dissociation of "proximal"- and "distal"-cue-based behaviors.
Rudy, J. W., Stadler-Morris, S., & Albert, P. (1987) · Behavioral Neuroscience · doi:10.1037/0735-7044.101.1.62 · Cited by 229 · see citing works
Ontogeny of spatial navigation behaviors in the rat: Dissociation of "proximal"- and "distal"-cue-based behaviors.
Rudy, J. W., Stadler-Morris, S., & Albert, P. (1987) · Behavioral Neuroscience · doi:10.1037//0735-7044.101.1.62 · Cited by 227 · see citing works
Development of Visual Centers in the Primate Brain Depends on Binocular Competition Before Birth
RAKIC, P. T. (1981) · Science · doi:10.1126/science.7302569 · Cited by 224 · see citing works
The organization of spatial coding in the hippocampus: a study of neural ensemble activity
Eichenbaum, H., Wiener, S. I., Shapiro, M., & Cohen, N. J. (1989) · Journal of Neuroscience · doi:10.1523/jneurosci.09-08-02764.1989 · Cited by 221 · see citing works
Contextual conditioning and auditory cue conditioning dissociate during development.
Rudy, J. W. (1993) · Behavioral Neuroscience · doi:10.1037//0735-7044.107.5.887 · Cited by 220 · see citing works
Ontogeny of contextual fear conditioning in rats: Implications for consolidation, infantile amnesia, and hippocampal system function.
Rudy, J. W., & Morledge, P. (1994) · Behavioral Neuroscience · doi:10.1037/0735-7044.108.2.227 · Cited by 207 · see citing works
Stress Impairs LTP and Hippocampal‐Dependent Memorya
Diamond, D. M., & ROSE, G. M. (1994) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1994.tb39271.x · Cited by 195 · see citing works
Altered synaptic transmission in dentate gyrus of rats reared in complex environments: evidence from hippocampal slices maintained in vitro
Green, E. J., & Greenough, W. T. (1986) · Journal of Neurophysiology · doi:10.1152/jn.1986.55.4.739 · Cited by 180 · see citing works
Contextual conditioning and auditory cue conditioning dissociate during development.
Rudy, J. W. (1993) · Behavioral Neuroscience · doi:10.1037/0735-7044.107.5.887 · Cited by 173 · see citing works
Development of glutamate binding sites and their regulation by calcium in rat hippocampus
Baudry, M., Arst, D., Oliver, M. W., & LYNCH, G. S. (1981) · Developmental Brain Research · doi:10.1016/0165-3806(81)90092-4 · Cited by 154 · see citing works
Long-term potentiation of synaptic transmission in kitten visual cortex
Komatsu, Y., Fujii, K., Maeda, J. E. M. S., Sakaguchi, H., & Toyama, K. (1988) · Journal of Neurophysiology · doi:10.1152/jn.1988.59.1.124 · Cited by 144 · see citing works
Mechanism of altered synaptic strength due to experience: relation to long-term potentiation.
Foster, T. C., Gagné, J., & Massicotte, G. (1996) · Brain Research · doi:10.1016/0006-8993(96)00707-x · Cited by 131 · see citing works
Sequential dependencies regulate sensory evoked responses of single units in the rat hippocampus
Foster, T. C., Christian, E. P., Hampson, R. E., Campbell, K. A., & Deadwyler, S. A. (1987) · Brain Research · doi:10.1016/0006-8993(87)90361-1 · Cited by 128 · see citing works
Brief visual experience induces immediate early gene expression in the cat visual cortex.
Rosen, K. M., McCormack, M., Villa‐Komaroff, L., & Mower, G. D. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.12.5437 · Cited by 124 · see citing works
Developmental changes in synaptic properties in hippocampus of neonatal rats
Müller, D., Oliver, M. W., & LYNCH, G. S. (1989) · Developmental Brain Research · doi:10.1016/0165-3806(89)90063-1 · Cited by 124 · see citing works
Induction of c-fos mRNA in the brain and anterior pituitary gland by a novel environment.
Handa, R. J., Nunley, K. M., & Bollnow, M. R. (1993) · PubMed · Cited by 120 · see citing works
A critical period for long-term potentiation in the developing rat visual cortex
Perkins, A. T., & Teyler, T. J. (1988) · Brain Research · doi:10.1016/0006-8993(88)91478-3 · Cited by 117 · see citing works
Differential ontogeny of working memory and reference memory in the rat.
Green, R. J., & Stanton, M. E. (1989) · Behavioral Neuroscience · doi:10.1037//0735-7044.103.1.98 · Cited by 113 · see citing works
Effects of stress and long-term potentiation (LTP) on subsequent LTP and the theta burst response in the dentate gyrus
Shors, T. J., & Dryver, E. T. (1994) · Brain Research · doi:10.1016/0006-8993(94)90777-3 · Cited by 111 · see citing works
Changes in c-fos mRNA expression in rat brain during odor discrimination learning: differential involvement of hippocampal subfields CA1 and CA3
Hess, U., LYNCH, G. S., & Gall, C. M. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-07-04786.1995 · Cited by 110 · see citing works
Differential ontogeny of working memory and reference memory in the rat.
Green, R. J., & Stanton, M. E. (1989) · Behavioral Neuroscience · doi:10.1037/0735-7044.103.1.98 · Cited by 102 · see citing works
Maturation of Adrenal Stress Responsiveness in the Rat
Schoenfeld, N. M., LEATHEM, J. H., & Rabii, J. (2008) · Neuroendocrinology · doi:10.1159/000123058 · Cited by 97 · see citing works
Exposure to a novel environment interferes with the induction of hippocampal primed burst potentiation in the behaving rat
Diamond, D. M., Catherine Bennett, M., Stevens, K. E., Wilson, R. L., & Rose, G. M. (1990) · Psychobiology · doi:10.3758/bf03327243 · Cited by 94 · see citing works
The critical period for long-term potentiation in primary sensory cortex
Fox, K. D. (1995) · Neuron · doi:10.1016/0896-6273(95)90136-1 · Cited by 91 · see citing works
The time of origin of cells demonstrating glutamic acid decarboxylase-like immunoreactivity in the hippocampal formation of the rat
Amaral, D. G., & Kurz, J. (1985) · Neuroscience Letters · doi:10.1016/0304-3940(85)90211-3 · Cited by 88 · see citing works
Acute stress impairs (or induces) synaptic long‐term potentiation (LTP) but does not affect paired‐pulse facilitation in the stratum radiatum of rat hippocampus
Shors, T. J., & Thompson, R. F. (1992) · Synapse · doi:10.1002/syn.890110311 · Cited by 88 · see citing works
Accumulation of c-fos mRNA in rat hippocampus during acquisition of a brightness discrimination
Tischmeyer, W., Kaczmarek, L., Strauss, M., Jork, R., & Matthies, H. (1990) · Behavioral and Neural Biology · doi:10.1016/0163-1047(90)91366-j · Cited by 86 · see citing works
An in vivo study of the ontogeny of long-term potentiation (LTP) in the CA1 region and in the dentate gyrus of the rat hippocampal formation
Bekenstein, J. W., & Lothman, E. W. (1991) · Developmental Brain Research · doi:10.1016/0165-3806(91)90084-v · Cited by 82 · see citing works
Ontogenesis of learning: VI. Learned and unlearned responses to visual stimulation in the infant hooded rat
Moye, T. B., & Rudy, J. W. (1985) · Developmental Psychobiology · doi:10.1002/dev.420180505 · Cited by 68 · see citing works
Immunohistochemical study of the pattern of rapid expression of c‐fos protein in the visual cortex of dark‐reared kittens following initial exposure to light
Beaver, C. J., Mitchell, D. E., & Robertson, H. A. (1993) · The Journal of Comparative Neurology · doi:10.1002/cne.903330402 · Cited by 65 · see citing works
Absence of c-fos induction in neonatal rat brain after seizures
Schreiber, S. S., Tocco, G., Najm, I., Finch, C. E., Johnson, S. A., & Baudry, M. (1992) · Neuroscience Letters · doi:10.1016/0304-3940(92)90640-s · Cited by 61 · see citing works
Developmental increase in CA3-CA1 presynaptic function in the hippocampal slice
Dumas, T. C., & Foster, T. C. (1995) · Journal of Neurophysiology · doi:10.1152/jn.1995.73.5.1821 · Cited by 61 · see citing works
Hippocampal Mossy Fiber Development at the Ultrastructural Level
Stirling, R. V., & Bliss, T. (1978) · Progress in brain research · doi:10.1016/s0079-6123(08)61023-7 · Cited by 55 · see citing works
N‐Methyl‐D‐Aspartate Antagonists Block Fos‐Like Protein Expression Induced via Multiple Signaling Pathways in Cultured Cortical Neurons
Hisanaga, K., Sagar, S. M., & Sharp, F. R. (1992) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1992.tb10060.x · Cited by 55 · see citing works
Developmental regulation of Fos and Fos‐related antigens in cerebral cortex, striatum, hippocampus, and cerebellum of the rat
Alcantara, A. A., & Greenough, W. T. (1993) · The Journal of Comparative Neurology · doi:10.1002/cne.903340106 · Cited by 55 · see citing works
Early response genes as markers of neuronal activity and growth factor action.
Sagar, S. M., & Sharp, F. R. (1993) · PubMed · Cited by 50 · see citing works
Spatial learning in preweanling rats trained in a Morris water maze
Kraemer, P. J., & Randall, C. K. (1995) · Psychobiology · doi:10.3758/bf03327070 · Cited by 48 · see citing works
Differences in the induction of Fos protein in cat visual cortex during and after the critical period
Mower, G. D. (1994) · Molecular Brain Research · doi:10.1016/0169-328x(94)90376-x · Cited by 46 · see citing works
Complex patterns of immediate early gene induction in rat brain following brightness discrimination training and pseudotraining
Grimm, R., & Tischmeyer, W. (1997) · Behavioural Brain Research · doi:10.1016/s0166-4328(97)83330-x · Cited by 46 · see citing works
Immunohistochemistry of c‐fos in Mouse Brain During Postnatal Development: Basal Levels and Changing Response to Metrazol and Kainate Injection
Sakurai‐Yamashita, Y., Sassone‐Corsi, P., & Gombos, G. (1991) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1991.tb01672.x · Cited by 45 · see citing works
Ontogeny of Kainate‐Induced Gene Expression in Rat Hippocampus
Pennypacker, K. R., McMillian, M., DOUGLASS, J. O., & Hong, J. (1994) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.1994.62020438.x · Cited by 31 · see citing works
A developmental analysis of the learning and short-term-memory processes mediating performance in conditional-spatial discrimination problems
Castro, C. A., Paylor, R. E., & Rudy, J. W. (1987) · Psychobiology · doi:10.3758/bf03327287 · Cited by 27 · see citing works
Elevated basal AP-1 DNA binding activity in developing rat brain
Pennypacker, K. R., Dreyer, D. A., Hong, J., & McMillian, M. (1993) · Molecular Brain Research · doi:10.1016/0169-328x(93)90138-f · Cited by 24 · see citing works
Latent inhibition in preweanling rats
Kraemer, P. J., & Randall, C. K. (1992) · Psychobiology · doi:10.3758/bf03327166 · Cited by 12 · see citing works

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Spear, L. P. (2000) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(00)00014-2 · Cited by 5,433 · see citing works
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Herdegen, T., & Leah, J. D. (1998) · Brain Research Reviews · doi:10.1016/s0165-0173(98)00018-6 · Cited by 1,352 · see citing works
Adolescent cortical development: A critical period of vulnerability for addiction
Crews, F., He, J., & Hodge, C. (2007) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2006.12.001 · Cited by 1,091 · see citing works
Impulsivity, frontal lobes and risk for addiction
Crews, F. T., & Boettiger, C. A. (2009) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2009.04.018 · Cited by 679 · see citing works
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O’Connor, T. G., Rutter, M., Beckett, C., Keaveney, L., Kreppner, J. M., & the English and Romanian Adoptees Study Team (2000) · Child Development · doi:10.1111/1467-8624.00151 · Cited by 353 · see citing works
Unpacking the cognitive map: The parallel map theory of hippocampal function.
Jacobs, L. F., & Schenk, F. (2003) · Psychological Review · doi:10.1037/0033-295x.110.2.285 · Cited by 325 · see citing works
Involvement of hippocampal synaptic plasticity in age-related memory decline
Foster, T. C. (1999) · Brain Research Reviews · doi:10.1016/s0165-0173(99)00017-x · Cited by 314 · see citing works
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McCutcheon, J. E., & Marinelli, M. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.06648.x · Cited by 279 · see citing works
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Danglot, L., Triller, A., & Marty, S. (2006) · Hippocampus · doi:10.1002/hipo.20225 · Cited by 167 · see citing works
Mechanism for increased hippocampal synaptic strength following differential experience.
Foster, T. C., & Dumas, T. C. (2001) · Journal of Neurophysiology · doi:10.1152/jn.2001.85.4.1377 · Cited by 111 · see citing works
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 · see citing works
Enriched Environment Prevents Hypobaric Hypoxia Induced Memory Impairment and Neurodegeneration: Role of BDNF/PI3K/GSK3β Pathway Coupled with CREB Activation
Jain, V., Baitharu, I., Prasad, D. N., & Ilavazhagan, G. (2013) · PLoS ONE · doi:10.1371/journal.pone.0062235 · Cited by 86 · see citing works
Retracted
Time‐dependent inhibition of hippocampal LTP in vitro following contextual fear conditioning in the rat
Sacchetti, B., Lorenzini, C. A., Baldi, E., Bucherelli, C., Roberto, M., Tassoni, G., & Brunelli, M. (2002) · European Journal of Neuroscience · doi:10.1046/j.0953-816x.2001.01844.x · Cited by 78 · see citing works
The intellectual disability gene Kirrel3 regulates target-specific mossy fiber synapse development in the hippocampus
Martin, E. A., Muralidhar, S., Wang, Z., Cervantes, D. C., Basu, R., Taylor, M. R., Hunter, J., Cutforth, T., Wilke, S. A., Ghosh, A., et al. (2015) · eLife · doi:10.7554/elife.09395 · Cited by 73 · see citing works
Induction of c‐Fos‐like and FosB‐like immunoreactivity reveals forebrain neuronal populations involved differentially in pup‐mediated maternal behavior in juvenile and adult rats
Kalinichev, M., Rosenblatt, J. S., Nakabeppu, Y., & Morrell, J. I. (2000) · The Journal of comparative neurology · doi:10.1002/(sici)1096-9861(20000103)416:1 · Cited by 72 · see citing works
Differential regulation of psychostimulant‐induced gene expression of brain derived neurotrophic factor and the immediate‐early geneArcin the juvenile and adult brain
Banerjee, P. S., Aston, J., Khundakar, A. A., & Zetterström, T. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2008.06601.x · Cited by 61 · see citing works
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Clinton, S. M., Stead, J. D. H., Miller, S., Watson, S. J., & Akil, H. (2011) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2011.07811.x · Cited by 58 · see citing works
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Gagné, J., Gélinas, S., Martinoli, M., Foster, T. C., Ohayon, M. M., Thompson, R. F., Baudry, M., & Massicotte, G. (1998) · Brain Research · doi:10.1016/s0006-8993(98)00451-x · Cited by 56 · see citing works
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Blair, M. G., Nguyen, N. N. Q., Albani, S. H., L'Etoile, M. M., Andrawis, M. M., Owen, L. M., Oliveira, R. F., Johnson, M. W., Purvis, D. L., Sanders, E. M., et al. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.4827-12.2013 · Cited by 55 · see citing works
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Crews, F. T., & Vetreno, R. P. (2011) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2011.00019 · Cited by 52 · see citing works
Regulation of synaptic plasticity in memory and memory decline with aging
Foster, T. C. (2002) · Progress in brain research · doi:10.1016/s0079-6123(02)38083-x · Cited by 51 · see citing works
Differential neuronal plasticity in mouse hippocampus associated with various periods of enriched environment during postnatal development
Hosseiny, S., Piétri, M., Petit-Paitel, A., Zarif, H., Heurteaux, C., Chabry, J., & Guyon, A. (2014) · Brain Structure and Function · doi:10.1007/s00429-014-0865-y · Cited by 49 · see citing works
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Dumas, T. C. (2004) · Developmental Psychobiology · doi:10.1002/dev.20011 · Cited by 38 · see citing works
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Kumar, A., & Foster, T. C. (2006) · Brain Research · doi:10.1016/j.brainres.2006.10.037 · Cited by 36 · see citing works
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Dumas, T. C. (2010) · Hippocampus · doi:10.1002/hipo.20881 · Cited by 33 · see citing works
Receptor blockade reveals a correspondence between hippocampal-dependent behavior and experience-dependent synaptic enhancement
Foster, T. C., Fugger, H. N., & Cunningham, S. (2000) · Brain Research · doi:10.1016/s0006-8993(00)02379-9 · Cited by 32 · see citing works
Central thalamic deep-brain stimulation alters striatal-thalamic connectivity in cognitive neural behavior
Lin, H.-C., Pan, H.-C., Lin, S.-H., Lo, Y.-C., Shen, E. T.-H., Liao, L.-D., Liao, P.-H., Chien, Y.-W., Liao, K.-D., Jaw, F.-S., et al. (2016) · Frontiers in Neural Circuits · doi:10.3389/fncir.2015.00087 · Cited by 29 · see citing works
Persistent downregulation of hippocampal CREB mRNA parallels a Y‐maze deficit in adolescent rats following semi‐chronic amphetamine administration
Featherby, T. J., van den Buuse, M., Lubman, D. I., & Lawrence, A. J. (2008) · British Journal of Pharmacology · doi:10.1038/bjp.2008.126 · Cited by 25 · see citing works
Light deprivation improves melatonin related suppression of hippocampal plasticity
Talaei, S. A., Sheibani, V., & Salami, M. (2010) · Hippocampus · doi:10.1002/hipo.20650 · Cited by 27 · see citing works
Tone conditioning potentiates rather than overshadows context fear in adult animals following adolescent ethanol exposure
Broadwater, M., & SPEAR, L. P. (2013) · Developmental Psychobiology · doi:10.1002/dev.21186 · Cited by 13 · see citing works
Postnatal development and sensory experience synergistically underlie the excitatory/inhibitory features of hippocampal neural circuits: glutamatergic and GABAergic neurotransmission
Talaei, S. A., Azami, A., & Salami, M. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2016.01.024 · Cited by 10 · see citing works
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Zarif, H., Nicolas, S., Petit-Paitel, A., Chabry, J., & Guyon, A. (2018) · InTech eBooks · doi:10.5772/intechopen.71426 · Cited by 8 · see citing works
Sensory experience differentially underlies developmental alterations of LTP in CA1 area and dentate gyrus
Talaei, S. A., & Salami, M. (2013) · Brain Research · doi:10.1016/j.brainres.2013.08.060 · Cited by 8 · see citing works
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Korshunova, I., Gjørlund, M. D., Owczarek, S., Petersen, A. V., Perrier, J., Gøtzsche, C. R., & Berezin, V. (2015) · Pharmacology Research & Perspectives · doi:10.1002/prp2.126 · Cited by 7 · see citing works
Light deprivation related changes of strategy selection in the radial arm maze
Salami, M. (2007) · Physiological Research · doi:10.33549/physiolres.930838 · Cited by 4 · see citing works
Ameliorative Effect of Moringa oleifera Against CUMS-Induced Anxiety in Rats: β-Catenin and 5-HT1 A Crosstalk
El‐Kadi, R. A., Sedeek, M. S., Abdelkader, N. F., Zaki, H. F., & Kamel, A. S. E. D. (2025) · Molecular Neurobiology · doi:10.1007/s12035-025-04911-8 · Cited by 4 · see citing works
Post-weaning mice fed exclusively milk have deficits in induction of long-term depression in the CA1 hippocampal region and spatial learning and memory
Nishie, H., Miyata, R., Fujikawa, R., Kinoshita, K.-I., Muroi, Y., & Ishii, T. (2012) · Neuroscience Research · doi:10.1016/j.neures.2012.05.006 · Cited by 3 · see citing works
Interaction of visual experience and melatonin in the spatial task learning
Salami, M., Talaei, S. A., Davari, S., & Hamidi, G. A. (2011) · Biological Rhythm Research · doi:10.1080/09291016.2011.593849 · Cited by 2 · see citing works
Dark and light rearing during early postnatal life impairs spatial learning of rats in Morris water maze
Talaei, S. A., Davari, S., & Salami, M. (2010) · Archives of Advances in Biosciences · doi:10.22037/jps.v1i4.2261 · Cited by 1 · see citing works
Wahrnehmungsdimensionen des haptischen Systems
Müller, S. M., & Grunwald, M. (2022) · Springer eBooks · doi:10.1007/978-3-662-64012-8_1 · Cited by 1 · see citing works
On the role of the hippocampus in the acquisition, long-term retention and semanticisation of memory
Gingell, S. (2005) · ERA
Evaluating effects of light deprivation on synaptic plasticity of hippocampal dentate gyrus neurons in rat
Talaei, S. A., Salami, M., & Banitaba, S. M. (2014)
Participation In A Movement Program and Its Impact on Pre-Academics: Pre-Literacy
Hoppe, J. (2016)
Perceptual Dimensions of the Haptic System
Mueller, S. M., & Grunwald, M. (2023) · Springer eBooks · doi:10.1007/978-3-662-67860-2_1
Modulation de la plasticité hippocampique par l’enrichissement de l’environnement : rôle des lymphocytes T
Zarif, H. (2017) · theses.fr (ABES) · doi:10.70675/100c0a4dzccb0z474cz8e5cze96f6d9cfe67
Untitled work
(2000) · doi:10.1002/(sici)1098-1063(2000)10:1

Environmental novelty is associated with a selective increase in Fos expression in the output elements of the hippocampal formation and the perirhinal cortexPreprint
VanElzakker, M. B., Fevurly, R. D., Breindel, T., & Spencer, R. L. (2008) · Learning & Memory · doi:10.1101/lm.1196508 · Cited by 179 · see citing works
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 · see citing works
Early eyelid opening enhances spontaneous alternation and accelerates the development of perforant path synaptic strength in the hippocampus of juvenile rats
Dumas, T. C. (2004) · Developmental Psychobiology · doi:10.1002/dev.20011 · Cited by 38 · see citing works
A critical period for learning and plastic changes at hippocampal CA1 synapses
Sakimoto, Y., Shintani, A., Yoshiura, D., Goshima, M., Kida, H., & Mitsushima, D. (2022) · Scientific Reports · doi:10.1038/s41598-022-10453-z · Cited by 23 · see citing works
Neonatal Exposure to Novel Environment Enhances Hippocampal-Dependent Memory Function During Infancy and AdulthoodPreprint
Tang, A. C. (2001) · Learning & Memory · doi:10.1101/lm.43101 · Cited by 101 · see citing works

Authors: Waters, N. S., Klintsova, A. Y., & Foster, T. C.
Affiliations: University of Virginia (US)
University of Illinois Urbana-Champaign (US)
ORCID: Klintsova, Anna Y.
Foster, Thomas C.
Venue: The Journal of Neuroscience
Publisher: Society for Neuroscience
Published: 1997-10-15
Volume: 17
Issue: 20
Pages: 7967-7973
ISSN: 0270-6474 (ISSN-L)
1529-2401
DOI: 10.1523/jneurosci.17-20-07967.1997
PMC: PMC6793919
OpenAlex: W2147622058
Cited by: 46
References: 69
Citations by year: 2025: 1 · 2023: 1 · 2022: 1 · 2018: 1 · 2017: 1 · 2016: 3 · 2015: 2 · 2014: 2 · 2013: 4 · 2012: 1
FWCI: 1.82
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by-nc-sa
creativecommons.org/licenses/by-nc-sa/4.0/ (vor, 182 d)
Locations: Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: National Institute of Neurological Disorders and Stroke (F32NS010115, NS31830, NS10115)
Eunice Kennedy Shriver National Institute of Child Health and Human Development (T32HD007323, HD07323)
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords: hippocampus, postnatal development, environmental enrichment, sensitive period, synaptic plasticity, long-term potentiation, Fos-like immunoreactivity, spontaneous alternation, CA1, hippocampal development
MeSH terms: Aging, Animals, Animals, Newborn, Behavior, Animal, Electrophysiology, Environment, Hippocampus, Immunohistochemistry, Male, Synaptic Transmission, Physical Stimulation, Proto-Oncogene Proteins c-fos, Rats, Sprague-Dawley, Long-Term Potentiation, Rats

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Insensitivity of the hippocampus to environmental stimulation during postnatal development

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