Learning deficit in BDNF mutant mice.
Abstract
Brain-derived neurotrophic factor (BDNF) has been implicated in the regulation of high-frequency synaptic transmission and long-term potentiation in the hippocampus, processes that are also thought to be involved in the learning of spatial tasks such as the Morris water maze. In order to determine whether BDNF is required for normal spatial learning, mice carrying a deletion in one copy of the BDNF gene were subjected to the Morris water maze task. Young adult BDNF mutant mice were significantly impaired compared with wild-type mice, requiring twice the number of days to reach full performance. Aged wild-type mice performed significantly worse than young wild-type mice and the effect was even more pronounced in the BDNF mutant mice, which did not learn at all. Although there was no difference in mean swimming speed between BDNF mutant and wild-type mice, we cannot exclude the possibility that developmental or peripheral deficits also contribute to the learning deficits in these mice. In situ hybridization and RNase protection analysis revealed that BDNF mRNA expression was indeed decreased in BDNF mutant mice. Furthermore, a pronounced effect of age on BDNF mRNA expression was seen, displayed as both a reduced level of mRNA expression and a reduced or entirely absent layer-specific expression pattern in the cerebral cortex of aged animals. Thus, our data suggest that BDNF expression may be linked to learning.
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Manipulation of brain-derived neurotrophic factor expression directly impacts upon performance in spatial and contextual memory tasks.
“The importance of BDNF to hippocampal neuroplasticity is epitomized by animal studies, which have found that the manipulation of BDNF expression directly impacts upon performance in spatial and contextual memory tasks (Linnarsson et al., 1997; Alonso et al., 2002; Heldt et al., 2007; Peters et al., 2010), and also that the downregulation of BDNF inhibits AE induced improvements in spatial memory”
From Aerobic Exercise as a Tool to Improve Hippocampal Plasticity and Function in Humans: Practical Implications for Mental Health Treatment (2016) · cites this paper as Linnarsson et al., 1997
Cites
A synaptic model of memory: long-term potentiation in the hippocampus
Bliss, T. V. P., & Collingridge, G. L. (1993) · Nature · doi:10.1038/361031a0 · Cited by 11,566 · see citing works
Developments of a water-maze procedure for studying spatial learning in the rat
Morris, R. (1984) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(84)90007-4 · Cited by 7,180 · see citing works
Physiology of the Neurotrophins
Lewin, G. R., & Barde, Y. (1996) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.19.030196.001445 · Cited by 1,955 · see citing works
Neurotrophins and Neuronal Plasticity
Thoenen, H. (1995) · Science · doi:10.1126/science.270.5236.593 · Cited by 1,927 · see citing works
Hippocampal long-term potentiation is impaired in mice lacking brain-derived neurotrophic factor.
Korte, M., Carroll, P., Wolf, E., Brem, G., Thoenen, H., & Bonhoeffer, T. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.19.8856 · Cited by 1,426 · see citing works
Long-Lasting Neurotrophin-Induced Enhancement of Synaptic Transmission in the Adult Hippocampus
Kang, H., & Schuman, E. M. (1995) · Science · doi:10.1126/science.7886457 · Cited by 1,354 · see citing works
Patterson, S. L., Abel, T., Deuel, T. A. S., Martin, K. C., Rose, J. C., & Kandel, E. R. (1996) · Neuron · doi:10.1016/s0896-6273(00)80140-3 · Cited by 1,233 · see citing works
Figurov, A., Pozzo-Miller, L. D., Olafsson, P., Wang, T., & Lu, B. (1996) · Nature · doi:10.1038/381706a0 · Cited by 1,106 · see citing works
Mice lacking brain-derived neurotrophic factor develop with sensory deficits
Ernfors, P., Lee, K.-F., & Jaenisch, R. (1994) · Nature · doi:10.1038/368147a0 · Cited by 1,067 · see citing works
Self-citationRegional distribution of brain‐derived neurotrophic factor mRNA in the adult mouse brain.
Hofer, M., Pagliusi, S. R., Hohn, A., Leibrock, J., & Barde, Y. (1990) · The EMBO Journal · doi:10.1002/j.1460-2075.1990.tb07423.x · Cited by 1,017 · see citing works
A Requirement for Local Protein Synthesis in Neurotrophin-Induced Hippocampal Synaptic Plasticity
Kang, H., & Schuman, E. (1996) · Science · doi:10.1126/science.273.5280.1402 · Cited by 1,010 · see citing works
Neurotrophins regulate dendritic growth in developing visual cortex
McAllister, A. K., Lo, D. C., & Katz, L. C. (1995) · Neuron · doi:10.1016/0896-6273(95)90171-x · Cited by 959 · see citing works
BDNF mRNA is decreased in the hippocampus of individuals with Alzheimer's disease
Phillips, H. S., Hains, J. M., Armanini, M., Laramee, G. R., Johnson, S. A., & Winslow, J. W. (1991) · Neuron · doi:10.1016/0896-6273(91)90273-3 · Cited by 921 · see citing works
Zafra, F., Hengerer, B., Leibrock, J., Thoenen, H., & Lindholm, D. (1990) · The EMBO Journal · doi:10.1002/j.1460-2075.1990.tb07564.x · Cited by 897 · see citing works
Gene-targeting studies of mammalian behavior: is it the mutation or the background genotype?
Gerlai, R. (1996) · Trends in Neurosciences · doi:10.1016/s0166-2236(96)20020-7 · Cited by 881 · see citing works
Multiple promoters direct tissue-specific expression of the rat BDNF gene
Timmusk, T., Palm, K., Metsis, M., Reintam, T., Paalme, V., Saarma, M., & Persson, H. (1993) · Neuron · doi:10.1016/0896-6273(93)90335-o · Cited by 858 · see citing works
Ernfors, P., Wetmore, C., Olson, L., & Persson, H. (1990) · Neuron · doi:10.1016/0896-6273(90)90090-3 · Cited by 819 · see citing works
Self-citationPotentiation of developing neuromuscular synapses by the neurotrophins NT-3 and BDNF
Lohof, A. M., Ip, N. Y., & Poo, M.-M. (1993) · Nature · doi:10.1038/363350a0 · Cited by 755 · see citing works
Isackson, P. J., Huntsman, M. M., Murray, K. D., & Gall, C. M. (1991) · Neuron · doi:10.1016/0896-6273(91)90234-q · Cited by 711 · see citing works
Levine, E. S., Dreyfus, C. F., Black, I. B., & Plummer, M. R. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.17.8074 · Cited by 611 · see citing works
Zafra, F., Ċastrén, E., Thoenen, H., & Lindholm, D. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.22.10037 · Cited by 580 · see citing works
Inhibition of Ocular Dominance Column Formation by Infusion of NT-4/5 or BDNF
Cabelli, R. J., Hohn, A., & Shatz, C. J. (1995) · Science · doi:10.1126/science.7886458 · Cited by 566 · see citing works
Synaptic development of the cerebral cortex: implications for learning, memory and mental illness
(1994) · Progress in Brain Research · doi:10.1016/s0079-6123(08)60543-9 · Cited by 565 · see citing works
Patterson, S. L., Grover, L. M., Schwartzkroin, P. A., & Bothwell, M. (1992) · Neuron · doi:10.1016/0896-6273(92)90067-n · Cited by 555 · see citing works
Widespread Expression of BDNF But Not NT3 by Target Areas of Basal Forebrain Cholinergic Neurons
PHILLIPS, H. S., Hains, J. M., Laramee, G. R., Rosenthal, A., & Winslow, J. W. (1990) · Science · doi:10.1126/science.1688328 · Cited by 532 · see citing works
Light regulates expression of brain-derived neurotrophic factor mRNA in rat visual cortex.
Castrén, E., Zafra, F., Thoenen, H., & Lindholm, D. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.20.9444 · Cited by 513 · see citing works
Spatial learning and motor deficits in aged rats
Gage, F. H., Dunnett, S. B., & Björklund, A. (1984) · Neurobiology of Aging · doi:10.1016/0197-4580(84)90084-8 · Cited by 508 · see citing works
BDNF, and NT-4/5 enhance glutamatergic synaptic transmission in cultured hippocampal neurones
Lemann, V., Gottmann, K., & Heumann, R. (1994) · NeuroReport · doi:10.1097/00001756-199412300-00007 · Cited by 402 · see citing works
Wetmore, C., Ernfors, P., Persson, H., & Olson, L. (1990) · Experimental Neurology · doi:10.1016/0014-4886(90)90068-4 · Cited by 367 · see citing works
Korte, M., Griesbeck, O., Gravel, C., Carroll, P., Staiger, V, Thoenen, H., & Bonhoeffer, T. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.22.12547 · Cited by 351 · see citing works
The induction of LTP increases BDNF and NGF mRNA but decreases NT-3 mRNA in the dentate gyrus
Castrén, E., Pitkänen, M., Sirviö, J., Parsadanian, A., Lindholm, D., Thoenen, H., & Riekkinen, P. J. (1993) · NeuroReport · doi:10.1097/00001756-199307000-00014 · Cited by 308 · see citing works
Otto, T., Eichenbaum, H., Wible, C. G., & Wiener, S. I. (1991) · Hippocampus · doi:10.1002/hipo.450010206 · Cited by 304 · see citing works
Neurotrophins and activity-dependent development of the neocortex
Bonhoeffer, T. (1996) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(96)80017-1 · Cited by 297 · see citing works
Biffo, S., Offenhäuser, N., Carter, B. D., & Barde, Y. (1995) · Development · doi:10.1242/dev.121.8.2461 · Cited by 270 · see citing works
Correlation between the Pharmacology of Long-Term Potentiation and the Pharmacology of Memory
Izquierdo, I., & Medina, J. H. (1995) · Neurobiology of Learning and Memory · doi:10.1006/nlme.1995.1002 · Cited by 230 · see citing works
Edwards, F. A. (1995) · Physiological Reviews · doi:10.1152/physrev.1995.75.4.759 · Cited by 179 · see citing works
Synaptic plasticity: hippocampal LTP
Larkman, A. U., & Jack, J. (1995) · Current Opinion in Neurobiology · doi:10.1016/0959-4388(95)80045-x · Cited by 174 · see citing works
Fischer, W., Sirevaag, A. M., Wiegand, S. J., Lindsay, R. M., & Björklund, A. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.18.8607 · Cited by 170 · see citing works
Synaptic structure and function: Dynamic organization yields architectural precision
Burns, M. E., & Augustine, G. J. (1995) · Cell · doi:10.1016/0092-8674(95)90160-4 · Cited by 164 · see citing works
Brain-derived neurotrophic factor expression after long-term potentiation
Dragunow, M., Beilharz, E. J., Mason, B., Lawlor, P. A., Abraham, W. C., & Gluckman, P. D. (1993) · Neuroscience Letters · doi:10.1016/0304-3940(93)90420-p · Cited by 156 · see citing works
Involvement of LTP in memory: Are we “searching under the street light”?
Barnes, C. A. (1995) · Neuron · doi:10.1016/0896-6273(95)90166-3 · Cited by 153 · see citing works
Schoups, A. A., Elliott, R. C., Friedman, W., & Black, I. B. (1995) · Developmental Brain Research · doi:10.1016/0165-3806(95)00043-d · Cited by 145 · see citing works
Ċastrén, E., Berzaghi, M. D. P., Lindholm, D., & Thoenen, H. (1993) · Experimental Neurology · doi:10.1006/exnr.1993.1124 · Cited by 101 · see citing works
Histology of the Nervous System
Guillery, R. W. (1996) · Trends in Neurosciences · doi:10.1016/s0166-2236(96)80029-4 · Cited by 76 · see citing works
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da Luz, A. C. D. D. S., Dias, G. P., Bevilaqua, M. C. D. N., Cocks, G. D., Gardino, P. F., Thuret, S., & Nardi, A. E. (2013) · Neuropsychobiology · doi:10.1159/000353269 · Cited by 4,012 · see citing works
Egan, M. F., Kojima, M., Callicott, J. H., Goldberg, T. E., Kolachana, B. S., Bertolino, A., Zaitsev, E., Gold, B., Goldman, D., Dean, M., et al. (2003) · Cell · doi:10.1016/s0092-8674(03)00035-7 · Cited by 3,888 · see citing works
Long-Term Potentiation and Memory
Lynch, M. A. (2004) · Physiological Reviews · doi:10.1152/physrev.00014.2003 · Cited by 2,001 · see citing works
Binder (2004) · doi:10.1080/08977190410001723308 · Cited by 1,481 · see citing works
Brain foods: The effects of nutrients on brain function.
Gómez-Pinilla, F. (2008) · Nature Reviews Neuroscience · doi:10.1038/nrn2421 · Cited by 1,372 · see citing works
BDNF function in adult synaptic plasticity: The synaptic consolidation hypothesis
Bramham, C. R., & Messaoudi, E. (2005) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2005.06.003 · Cited by 1,193 · see citing works
Neurotrophins: key regulators of cell fate and cell shape in the vertebrate nervous systemPreprint
Bibel, M., & Barde, Y. (2000) · Genes & Development · doi:10.1101/gad.841400 · Cited by 1,054 · see citing works
BDNF and synaptic plasticity, cognitive function, and dysfunction
Lu, B., Nagappan, G., & Lu, Y. (2014) · Handbook of Experimental Pharmacology · doi:10.1007/978-3-642-45106-5_9 · Cited by 1,043 · see citing works
BDNF and 5-HT: a dynamic duo in age-related neuronal plasticity and neurodegenerative disorders
Mattson, M. P., Maudsley, S., & Martin, B. (2004) · Trends in Neurosciences · doi:10.1016/j.tins.2004.08.001 · Cited by 942 · see citing works
Molteni, R., Barnard, R. J., Ying, Z., Roberts, C. K., & Gómez‐Pinilla, F. (2002) · Neuroscience · doi:10.1016/s0306-4522(02)00123-9 · Cited by 918 · see citing works
Murer, M. G., Yan, Q., & Raisman-Vozari, R. (2001) · Progress in Neurobiology · doi:10.1016/s0301-0082(00)00014-9 · Cited by 874 · see citing works
Essential Role for TrkB Receptors in Hippocampus-Mediated Learning
Minichiello, L., Korte, M., Wolfer, D., Kühn, R., Unsicker, K., Cestari, V., Rossi-Arnaud, C., Lipp, H.-P., Bonhoeffer, T., & Klein, R. (1999) · Neuron · doi:10.1016/s0896-6273(00)80853-3 · Cited by 799 · see citing works
BDNF regulates eating behavior and locomotor activity in mice
Kernie, S. G., Liebl, D. J., & Parada, L. F. (2000) · The EMBO Journal · doi:10.1093/emboj/19.6.1290 · Cited by 806 · see citing works
Epigenetic Regulation of <i>bdnf</i> Gene Transcription in the Consolidation of Fear Memory
Lubin, F. D., Roth, T. L., & Sweatt, J. D. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.1786-08.2008 · Cited by 793 · see citing works
A simple role for BDNF in learning and memory?
Cunha, C. (2010) · Frontiers in Molecular Neuroscience · doi:10.3389/neuro.02.001.2010 · Cited by 778 · see citing works
BDNF: A key regulator for protein synthesis-dependent LTP and long-term memory?
Lü, Y., Christian, K. M., & Lu, B. (2007) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2007.08.018 · Cited by 768 · see citing works
BDNF-based synaptic repair as a disease-modifying strategy for neurodegenerative diseases
Lu, B., Nagappan, G., Guan, X.-M., Nathan, P. J., & Wren, P. B. (2013) · Nature reviews. Neuroscience · doi:10.1038/nrn3505 · Cited by 747 · see citing works
BDNF-induced local protein synthesis and synaptic plasticity
Leal, G., Comprido, D., & Duarte, C. B. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.04.005 · Cited by 685 · see citing works
Essential role of brain-derived neurotrophic factor in adult hippocampal function
Monteggia, L. M., Barrot, M., Powell, C. M., Berton, O., Galanis, V., Gemelli, T., Meuth, S., Nagy, A., Greene, R. W., & Nestler, E. J. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0402141101 · Cited by 685 · see citing works
Heldt, S. A., Stanek, L., Chhatwal, J. P., & Ressler, K. J. (2007) · Molecular Psychiatry · doi:10.1038/sj.mp.4001957 · Cited by 684 · see citing works
Tyler, W. J., Alonso, M., Bramham, C. R., & Pozzo‐Miller, L. D. (2002) · Learning & Memory · doi:10.1101/lm.51202 · Cited by 679 · see citing works
Rapid and selective induction of BDNF expression in the hippocampus during contextual learning
Hall, J., Thomas, K. L., & Everitt, B. (2000) · Nature Neuroscience · doi:10.1038/75698 · Cited by 669 · see citing works
Brain-Derived Neurotrophic Factor/TrkB Signaling in Memory Processes
Yamada, K., & Nabeshima, T. (2003) · Journal of Pharmacological Sciences · doi:10.1254/jphs.91.267 · Cited by 585 · see citing works
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 · see citing works
Mizuno, M., Yamada, K., Olariu, A., Nawa, H., & NABESHIMA, T. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-18-07116.2000 · Cited by 549 · see citing works
Reduced brain-derived neurotrophic factor in prefrontal cortex of patients with schizophrenia
Weickert, C. S., Hyde, T. M., Lipska, B. K., Herman, M. M., Weinberger, D. R., & Kleinman, J. E. (2003) · Molecular Psychiatry · doi:10.1038/sj.mp.4001308 · Cited by 533 · see citing works
Wu, A., Ying, Z., & Gomez-Pinilla, F. (2004) · Journal of Neurotrauma · doi:10.1089/neu.2004.21.1457 · Cited by 518 · see citing works
BDNF as a Promising Therapeutic Agent in Parkinson’s Disease
Palasz, E., Wysocka, A., Gasiorowska, A., Chalimoniuk, M., Niewiadomski, W., & Niewiadomska, G. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21031170 · Cited by 504 · see citing works
Monteggia, L. M., Luikart, B., Barrot, M., Theobold, D., Malkovska, I., Nef, S., Parada, L. F., & Nestler, E. J. (2007) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.03.021 · Cited by 502 · see citing works
Roceri, M., Hendriks, W. J. A. J., Racagni, G., Ellenbroek, B. A., & Riva, M. A. (2002) · Molecular Psychiatry · doi:10.1038/sj.mp.4001036 · Cited by 465 · see citing works
Williams, C. M., Mohsen, M. A. E., Vauzour, D., Rendeiro, C., Butler, L. T., Ellis, J. A., Whiteman, M., & Spencer, J. P. E. (2008) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2008.04.008 · Cited by 426 · see citing works
Vaynman, S., & Gomez-Pinilla, F. (2005) · Neurorehabilitation and Neural Repair · doi:10.1177/1545968305280753 · Cited by 420 · see citing works
Noradrenergic mechanisms in neurodegenerative diseases: a theory
Marien, M. R., Colpaert, F. C., & Rosenquist, A. C. (2004) · Brain Research Reviews · doi:10.1016/j.brainresrev.2004.02.002 · Cited by 411 · see citing works
Regulation of hippocampal synaptic plasticity by BDNF
Leal, G., Afonso, P. M., Salazar, I. L., & Duarte, C. B. (2015) · Brain Research · doi:10.1016/j.brainres.2014.10.019 · Cited by 410 · see citing works
Wu, A., Ying, Z., & Gómez‐Pinilla, F. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03246.x · Cited by 402 · see citing works
Chen, Z.-Y., Ieraci, A., Teng, H. K., Dall, H., Meng, C.-X., Herrera, D. G., Nykjær, A., Hempstead, B. L., & Lee, F. S. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.1017-05.2005 · Cited by 401 · see citing works
Flavonoids: modulators of brain function?
Spencer, J. P. E. (2008) · British Journal Of Nutrition · doi:10.1017/s0007114508965776 · Cited by 385 · see citing works
Adachi, M., Barrot, M., Autry, A. E., Theobald, D., & Monteggia, L. M. (2008) · Biological Psychiatry · doi:10.1016/j.biopsych.2007.09.019 · Cited by 380 · see citing works
Gómez‐Pinilla, F., Vaynman, S., & Ying, Z. (2008) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2008.06524.x · Cited by 379 · see citing works
Ploughman, M., Windle, V., MacLellan, C. L., White, N., Doré, J. J. E., & Corbett, D. (2009) · Stroke · doi:10.1161/strokeaha.108.531806 · Cited by 362 · see citing works
Rattiner, L. M., Davis, M., French, C. T., & Ressler, K. J. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.5654-03.2004 · Cited by 360 · see citing works
Molteni, R., Wu, A., Vaynman, S., Ying, Z., Barnard, R. J., & Gómez‐Pinilla, F. (2003) · Neuroscience · doi:10.1016/j.neuroscience.2003.09.020 · Cited by 350 · see citing works
Zuena, A. R., Mairesse, J., Casolini, P., Cinque, C., Alemà, G., Morley‐Fletcher, S., Chiodi, V., Spagnoli, L. G., Gradini, R., Catalani, A., et al. (2008) · PLoS ONE · doi:10.1371/journal.pone.0002170 · Cited by 339 · see citing works
The longer-term impacts of Western diet on human cognition and the brain
Francis, H., & Stevenson, R. J. (2013) · Appetite · doi:10.1016/j.appet.2012.12.018 · Cited by 342 · see citing works
Pang, P. T., & Lu, B. (2004) · Ageing Research Reviews · doi:10.1016/j.arr.2004.07.002 · Cited by 337 · see citing works
Alonso, M., Vianna, M. R. M., Depino, A. M., Mello e Souza, T., Pereira, P., Szapiro, G., Viola, H., Pitossi, F., Izquierdo, I., & Medina, J. H. (2002) · Hippocampus · doi:10.1002/hipo.10035 · Cited by 339 · see citing works
Variant BDNF (Val66Met) impact on brain structure and function
Bath, K. G., & Lee, F. S. (2006) · Cognitive Affective & Behavioral Neuroscience · doi:10.3758/cabn.6.1.79 · Cited by 325 · see citing works
Physical exercise as an epigenetic modulator of brain plasticity and cognition
Fernandes, J., Arida, R. M., & Gómez‐Pinilla, F. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.06.012 · Cited by 326 · see citing works
Clinical relevance of the neurotrophins and their receptors
Allen, S. J., & Dawbarn, D. (2006) · Clinical Science · doi:10.1042/cs20050161 · Cited by 316 · see citing works
Croll, S. D., Suri, C., Compton, D. L., Simmons, M. V., Yancopoulos, G. D., Lindsay, R. M., Wiegand, S. J., Rudge, J., & Scharfman, H. E. (1999) · Neuroscience · doi:10.1016/s0306-4522(99)00296-1 · Cited by 310 · see citing works
Reviews: BDNF and Memory Formation and Storage
Bekinschtein, P., Cammarota, M., Izquierdo, I., & Medina, J. H. (2007) · The Neuroscientist · doi:10.1177/1073858407305850 · Cited by 309 · see citing works
Neurotrophin regulation of synaptic transmission
Schuman, E. M. (1999) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(99)80013-0 · Cited by 309 · see citing works
Vaynman, S., & Gomez‐Pinilla, F. (2006) · Journal of Neuroscience Research · doi:10.1002/jnr.20979 · Cited by 299 · see citing works
Wu, A., Ying, Z., & Gómez‐Pinilla, F. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.05.061 · Cited by 299 · see citing works
Wu, A., Ying, Z., & Gómez‐Pinilla, F. (2006) · Experimental Neurology · doi:10.1016/j.expneurol.2005.09.004 · Cited by 292 · see citing works
Role of the brain‐derived neurotrophic factor at glutamatergic synapses
Carvalho, A. L., Caldeira, M. V., Santos, S. D., & Duarte, C. B. (2008) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0707509 · Cited by 290 · see citing works
Devi, L., & Ohno, M. (2012) · Neuropsychopharmacology · doi:10.1038/npp.2011.191 · Cited by 282 · see citing works
Mu, J.-S., Li, W., Yao, Z., & Zhou, X. (1999) · Brain Research · doi:10.1016/s0006-8993(99)01592-9 · Cited by 282 · see citing works
Role of BDNF in bipolar and unipolar disorder: Clinical and theoretical implications
Post, R. M. (2007) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2006.09.009 · Cited by 286 · see citing works
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
Environmental enrichment and the brain
Mohammed, A. H., Zhu, S., Darmopil, S., Hjerling‐Leffler, J., Ernfors, P., Winblad, B. G., Diamond, M. C., Eriksson, P. S., & Bogdanović, N. (2002) · Progress in brain research · doi:10.1016/s0079-6123(02)38074-9 · Cited by 267 · see citing works
Bekinschtein, P., Oomen, C., Saksida, L., & Bussey, T. (2011) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2011.07.002 · Cited by 86 · see citing works
Exercise influence on the microbiome–gut–brain axis
Dalton, A., Mermier, C. M., & Zuhl, M. (2019) · Gut Microbes · doi:10.1080/19490976.2018.1562268 · Cited by 261 · see citing works
Relative Contribution of Endogenous Neurotrophins in Hippocampal Long-Term Potentiation
Chen, G., Kolbeck, R., Barde, Y., Bonhoeffer, T., & Kossel, A. H. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-18-07983.1999 · Cited by 244 · see citing works
Is Serum Brain-Derived Neurotrophic Factor a Biomarker for Cognitive Enhancement in Schizophrenia?
Vinogradov, S., Fisher, M., Holland, C. M., Shelly, W. B., Wolkowitz, O. M., & Mellon, S. H. (2009) · Biological Psychiatry · doi:10.1016/j.biopsych.2009.02.017 · Cited by 241 · see citing works
An unliganded thyroid hormone receptor causes severe neurological dysfunction
Hashimoto, K., Curty, F. H., Borges, P. P., Lee, C. E., Abel, E. D., Elmquist, J. K., Cohen, R., & Wondisford, F. E. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.051454698 · Cited by 239 · see citing works
Wu, A., Molteni, R., Ying, Z., & Gómez‐Pinilla, F. (2003) · Neuroscience · doi:10.1016/s0306-4522(03)00154-4 · Cited by 223 · see citing works
The Gut-Brain Axis, BDNF, NMDA and CNS Disorders
Maqsood, R., & Stone, T. W. (2016) · Neurochemical Research · doi:10.1007/s11064-016-2039-1 · Cited by 223 · see citing works
The impact of flavonoids on memory: physiological and molecular considerations
Spencer, J. P. E. (2009) · Chemical Society Reviews · doi:10.1039/b800422f · Cited by 219 · see citing works
Learning deficits in forebrain-restricted brain-derived neurotrophic factor mutant mice
Gorski, J. A., Balogh, S. A., Wehner, J. M., & Jones, K. R. (2003) · Neuroscience · doi:10.1016/s0306-4522(03)00426-3 · Cited by 218 · see citing works
BDNF and trkB mRNA expression in the hippocampus and temporal cortex during the human lifespan
Webster, M. J., Herman, M. M., Kleinman, J. E., & Weickert, C. S. (2006) · Gene Expression Patterns · doi:10.1016/j.modgep.2006.03.009 · Cited by 218 · see citing works
Tsai, S., Cheng, C., Yu, Y. W., Chen, T., & Hong, C. (2003) · American Journal of Medical Genetics Part B Neuropsychiatric Genetics · doi:10.1002/ajmg.b.20026 · Cited by 213 · see citing works
MacQUEEN, G. M., Ramakrishman, K., Croll, S. D., Siuciak, J. A., Yu, G., Young, T., & Fahnestock, M. L. (2001) · Behavioral Neuroscience · doi:10.1037/0735-7044.115.5.1145 · Cited by 212 · see citing works
Integrin Requirement for Hippocampal Synaptic Plasticity and Spatial Memory
Chan, C.-S., Weeber, E. J., Kurup, S., Sweatt, J. D., & Davis, R. L. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-18-07107.2003 · Cited by 202 · see citing works
Spencer, J. P. E. (2008) · Proceedings of The Nutrition Society · doi:10.1017/s0029665108007088 · Cited by 195 · see citing works
Duan, W., Guo, Z., Jiang, H., Ware, M., & Mattson, M. P. (2003) · Endocrinology · doi:10.1210/en.2002-0113 · Cited by 194 · see citing works
Chapter 3 Activity-dependent regulation of neuronal plasticity and self repair
Kempermann, G., van Praag, H., & Gage, F. H. (2000) · Progress in brain research · doi:10.1016/s0079-6123(00)27004-0 · Cited by 189 · see citing works
Novkovic, T., Mittmann, T., & Manahan‐Vaughan, D. (2014) · Hippocampus · doi:10.1002/hipo.22342 · Cited by 189 · see citing works
Nithianantharajah, J. (2004) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2004.02.002 · Cited by 191 · see citing works
Brain-Derived Neurotrophic Factor Plays a Critical Role in Contextual Fear Conditioning
Liu, I. Y. C., Lyons, W. E., Mamounas, L. A., & Thompson, R. F. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.1948-04.2004 · Cited by 190 · see citing works
Memory inhibition and energy regulation
Davidson, T. L., Kanoski, S. E., Walls, E. K., & Jarrard, L. E. (2005) · Physiology & Behavior · doi:10.1016/j.physbeh.2005.09.004 · Cited by 183 · see citing works
BDNF Protects against Spatial Memory Deficits Following Neonatal Hypoxia-Ischemia
Almli, C. R., Levy, T. J., Han, B. H., Shah, A. R., Gidday, J. M., & Holtzman, D. M. (2000) · Experimental Neurology · doi:10.1006/exnr.2000.7492 · Cited by 186 · see citing works
The role of eicosanoids in the brain.
Tassoni, D., Kaur, G., Weisinger, R. S., & Sinclair, A. J. (2008) · PubMed · Cited by 184 · see citing works
Epigenetics and the Biological Basis of Gene × Environment Interactions
Bagot, R. C., & Meaney, M. J. (2010) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1016/j.jaac.2010.06.001 · Cited by 177 · see citing works
The Neurotrophins and Their Role in Alzheimers Disease
Allen, S. J., Watson, J. J., & Dawbarn, D. (2011) · Current Neuropharmacology · doi:10.2174/157015911798376190 · Cited by 177 · see citing works
Oxidative Stress in Cognitive and Epigenetic Aging: A Retrospective Glance
Kandlur, A., Satyamoorthy, K., & Gangadharan, G. (2020) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2020.00041 · Cited by 177 · see citing works
Koponen, E., Võikar, V., Riekki, R., Saarelainen, T., Rauramaa, T., Rauvala, H., Taira, T., & Castrén, E. (2004) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2004.01.006 · Cited by 170 · see citing works
The mouse: genetics meets behaviour
Bućan, M., & Abel, T. G. (2002) · Nature Reviews Genetics · doi:10.1038/nrg728 · Cited by 170 · see citing works
Callaghan, B. L., & Richardson, R. (2011) · Behavioral Neuroscience · doi:10.1037/a0022008 · Cited by 169 · see citing works
Gobbo, O. L., & O’Mara, S. M. (2003) · Behavioural Brain Research · doi:10.1016/j.bbr.2003.10.017 · Cited by 170 · see citing works
Cirulli, F., Berry, A., Chiarotti, F., & Alleva, E. (2004) · Hippocampus · doi:10.1002/hipo.10220 · Cited by 167 · see citing works
Macbeth, A. H., & Luine, V. N. (2009) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2009.08.011 · Cited by 169 · see citing works
Chourbaji, S., Hellweg, R., Brandis, D., Zörner, B., Zacher, C., Lang, U. E., Henn, F. A., Hörtnagl, H., & Gass, P. (2004) · Molecular Brain Research · doi:10.1016/j.molbrainres.2003.11.002 · Cited by 165 · see citing works
Wu, A., Ying, Z., & Gómez‐Pinilla, F. (2009) · Neurorehabilitation and neural repair · doi:10.1177/1545968309348318 · Cited by 164 · see citing works
Teixeira, A. L., Barbosa, I. G., Diniz, B. S., & Kümmer, A. (2010) · Biomarkers in Medicine · doi:10.2217/bmm.10.111 · Cited by 162 · see citing works
Viviani, B., Bartesaghi, S., Corsini, E., Villa, P., Ghezzi, P., Garau, A., Galli, C. L., & Marinovich, M. (2005) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2005.03033.x · Cited by 165 · see citing works
Spinal Plasticity and Behavior: BDNF-Induced Neuromodulation in Uninjured and Injured Spinal Cord
Garraway, S. M., & Huie, J. R. (2016) · Neural Plasticity · doi:10.1155/2016/9857201 · Cited by 158 · see citing works
Modulation of hippocampal synaptic transmission and plasticity by neurotrophins
Lu, B., & Gottschalk, W. (2000) · Progress in brain research · doi:10.1016/s0079-6123(00)28020-5 · Cited by 158 · see citing works
Pattwell, S. S., Bath, K. G., Perez-Castro, R., Lee, F. S., Chao, M. V., & Ninan, I. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.5205-11.2012 · Cited by 156 · see citing works
Kondo, M., Takei, Y., & Hirokawa, N. (2012) · Neuron · doi:10.1016/j.neuron.2011.12.020 · Cited by 156 · see citing works
- Authors
- Linnarsson, S., Björklund, A., & Ernfors, P.
- Affiliations
- Karolinska Institutet (SE)
- Lund University (SE)
- Corresponding author
- Linnarsson, Sten
- Venue
- European Journal of Neuroscience
- Publisher
- Wiley
- Published
- 1997-12
- Volume
- 9
- Issue
- 12
- Pages
- 2581-2587
- ISSN
- 0953-816X (ISSN-L)
- 1460-9568
- OpenAlex
- W2136761139
- Cited by
- 471
- References
- 44
- Citations by year
- 2026: 3 · 2025: 5 · 2024: 7 · 2023: 12 · 2022: 10 · 2021: 9 · 2020: 11 · 2019: 12 · 2018: 9 · 2017: 16 · 2016: 20 · 2015: 25 · 2014: 25 · 2013: 29 · 2012: 30
- FWCI
- 3.15
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- European Journal of Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Cancerfonden
- Vetenskapsrådet
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Nerve injury and regeneration
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- brain-derived neurotrophic factor, BDNF knockout mice, spatial learning, Morris water maze, hippocampus, long-term potentiation, synaptic transmission, BDNF mRNA expression, age-related decline, cerebral cortex, learning deficits
- MeSH terms
- Age Factors, Animals, Mice, Inbred BALB C, Mice, Neurologic Mutants, Retention, Psychology, RNA, Messenger, Spatial Behavior, Long-Term Potentiation, Gene Expression Regulation, Developmental, Maze Learning, Brain-Derived Neurotrophic Factor, Mice
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