From Acquisition to Consolidation: On the Role of Brain-Derived Neurotrophic Factor Signaling in Hippocampal-Dependent Learning

Learning and Memory - Tập 9 Số 5 - Trang 224-237 - 2002
William J. Tyler1,2,3, Mariana Alonso1,2,3, Clive R. Bramham1,2,3, Lucas Pozzo‐Miller1,2,3
12Instituto de Biología Celular y Neurociencias, Facultad de Medicina, Universidad de Buenos Aires, Buenos Aires, Argentina
23Department of Physiology and Locus on Neuroscience, University of Bergen, N-5009 Bergen, Norway
3Departments of Neurobiology and Psychology, Civitan International Research Center, University of Alabama at Birmingham, Birmingham, Alabama 35294-0021, USA

Tóm tắt

One of the most rigorously investigated problems in modern neuroscience is to decipher the mechanisms by which experience-induced changes in the central nervous system are translated into behavioral acquisition, consolidation, retention, and subsequent recall of information. Brain-derived neurotrophic factor (BDNF) has recently emerged as one of the most potent molecular mediators of not only central synaptic plasticity, but also behavioral interactions between an organism and its environment. Recent experimental evidence indicates that BDNF modulates synaptic transmission and plasticity by acting across different spatial and temporal domains. BDNF signaling evokes both short- and long-term periods of enhanced synaptic physiology in both pre- and postsynaptic compartments of central synapses. Specifically, BDNF/TrkB signaling converges on the MAP kinase pathway to enhance excitatory synaptic transmission in vivo, as well as hippocampal-dependent learning in behaving animals. Emerging concepts of the intracellular signaling cascades involved in synaptic plasticity induced through environmental interactions resulting in behavioral learning further support the contention that BDNF/TrkB signaling plays a fundamental role in mediating enduring changes in central synaptic structure and function. Here we review recent literature showing the involvement of BDNF/TrkB signaling in hippocampal-dependent learning paradigms, as well as in the types of cellular plasticity proposed to underlie learning and memory.

Từ khóa


Tài liệu tham khảo

10.1016/S0959-4388(00)00194-X

10.1016/0092-8674(93)90614-V

10.1073/pnas.95.19.11429

10.1016/S0006-8993(99)01748-5

10.1002/hipo.10035

10.1146/annurev.ph.55.030193.002145

Bain A. (1872) Mind and body: The theories of their relation. (Henry S. King, London).

10.1016/0014-4886(91)90082-N

10.1038/378182a0

Bao, 1998, Impaired eye-blink conditioning in waggler, a mutant mouse with cerebellar BDNF deficiency., Learn. Mem., 5, 355, 10.1101/lm.5.4.355

Berninger, 1995, GABAergic stimulation switches from enhancing to repressing BDNF expression in rat hippocampal neurons during maturation in vitro., Development, 121, 2327, 10.1242/dev.121.8.2327

10.1146/annurev.neuro.24.1.139

10.1002/(SICI)1097-4695(199910)41:1<108::AID-NEU14>3.0.CO;2-U

10.1016/0092-8674(94)90400-6

10.1002/(SICI)1096-9861(19960506)368:3<371::AID-CNE4>3.0.CO;2-2

Bramham C.R. Messaoudi E. Bårdsen K. (2002) Neurotrophins and synaptic plasticity in the adult hippocampus. in Site-selective neurotoxicity, ed Lester D.S. (Taylor and Francis, London, UK), pp 61–77.

10.1126/science.7886458

Cajal S. Ramón y (1909) Histologie du Système Nerveux de l'Homme et des Vertébrés. (Maloine, Paris) . (Reprinted in 1952 by Consejo Superior de Investigaciones Científicas, Instituto Ramón y Cajal, Madrid.).

10.1097/00001756-199307000-00014

10.1016/S0304-3940(00)01173-3

Conner, 1997, Distribution of brain-derived neurotrophic factor (BDNF) protein and mRNA in the normal adult rat CNS: Evidence for anterograde axonal transport., J. Neurosci., 17, 2295, 10.1523/JNEUROSCI.17-07-02295.1997

10.1016/S0306-4522(99)00296-1

10.1101/lm.6.3.257

da Penha Berzaghi, 1993, Cholinergic regulation of brain-derived neurotrophic factor (BDNF) and nerve growth factor (NGF) but not neurotrophin-3 (NT-3) mRNA levels in the developing rat hippocampus., J. Neurosci., 13, 3818, 10.1523/JNEUROSCI.13-09-03818.1993

10.1016/0304-3940(93)90420-P

Drake, 1999, Ultrastructural localization of full-length trkB immunoreactivity in rat hippocampus suggests multiple roles in modulating activity-dependent synaptic plasticity., J. Neurosci., 19, 8009, 10.1523/JNEUROSCI.19-18-08009.1999

10.1038/19978

10.1016/0896-6273(91)90084-D

10.1016/0304-3940(92)90494-R

10.1074/jbc.272.14.8837

10.1038/381706a0

10.1016/S0896-6273(00)80395-5

10.1073/pnas.91.18.8607

Foster M. Sherringhton C.S. (1897) A text book of physiology. Part III. The central nervous system. (Macmillan, London).

French, 1999, Hippocampal neurotrophin and trk receptor mRNA levels are altered by local administration of nicotine, carbachol and pilocarpine., Brain Res. Mol. Brain Res., 67, 124, 10.1016/S0169-328X(99)00048-0

Gallo, 1998, Localized sources of neurotrophins initiate axon collateral sprouting., J. Neurosci., 18, 5403, 10.1523/JNEUROSCI.18-14-05403.1998

10.1016/S0959-4388(99)00061-6

10.1037/0735-7044.116.3.455

10.1126/science.1361685

10.1016/0014-4886(73)90090-3

Guzowski, 2000, Inhibition of activity-dependent Arc protein expression in the rat hippocampus impairs the maintenance of long-term potentiation and the consolidation of long-term memory., J. Neurosci., 20, 3993, 10.1523/JNEUROSCI.20-11-03993.2000

10.1038/75698

10.1046/j.1460-9568.2000.00185.x

10.1093/emboj/20.21.5887

Haubensak, 1998, BDNF&NDASH;GFP containing secretory granules are localized in the vicinity of synaptic junctions of cultured cortical neurons., J. Cell Sci., 111, 1483, 10.1242/jcs.111.11.1483

Hebb D.O. (1949) The organization of behavior. (Wiley, New York).

10.1016/S0896-6273(00)80785-0

Horger, 1999, Enhancement of locomotor activity and conditioned reward to cocaine by brain-derived neurotrophic factor., J. Neurosci., 19, 4110, 10.1523/JNEUROSCI.19-10-04110.1999

10.1146/annurev.neuro.24.1.677

10.1016/0092-8674(95)90146-9

10.1006/exnr.2000.7415

10.1016/0896-6273(91)90234-Q

Iwasaki, 1998, Association of the Src family tyrosine kinase Fyn with TrkB., J. Neurochem., 71, 106, 10.1046/j.1471-4159.1998.71010106.x

10.1038/31371

James W. (1890) Principles of psychology. (Henry Holt, New York).

Jarvis, 1997, Neurotrophin modulation of NMDA receptors in cultured murine and isolated rat neurons., J. Neurophysiol., 78, 2363, 10.1152/jn.1997.78.5.2363

10.1016/S0306-4522(98)00362-5

10.1038/44847

10.1016/S0896-6273(00)80378-5

10.1002/neu.480251108

10.1037/0735-7044.112.4.1012

10.1111/j.1460-9568.1994.tb00312.x

10.1126/science.1057415

10.1002/jnr.1080

10.1073/pnas.90.14.6711

10.1073/pnas.92.19.8856

10.1073/pnas.93.22.12547

10.1016/S0028-3908(98)00035-5

10.1126/science.1067766

10.1016/0306-4522(93)90407-7

Lesser, 1997, Neurotrophins differentially regulate voltage-gated ion channels., Mol. Cell Neurosci., 10, 173, 10.1006/mcne.1997.0656

10.1073/pnas.92.17.8074

10.1073/pnas.95.17.10235

10.1016/S0169-328X(97)00349-5

10.1016/0736-5748(94)90054-X

10.1111/j.1460-9568.1997.tb01687.x

10.1016/S0306-4522(97)00325-4

10.1126/science.283.5409.1923

10.1146/annurev.neuro.23.1.649

Martinez, 1998, TrkB and TrkC signaling are required for maturation and synaptogenesis of hippocampal connections., J. Neurosci., 18, 7336, 10.1523/JNEUROSCI.18-18-07336.1998

10.1016/0896-6273(95)90171-X

10.1146/annurev.neuro.22.1.295

Messaoudi, 1998, Acute intrahippocampal infusion of BDNF induces lasting potentiation of synaptic transmission in the rat dentate gyrus., J. Neurophysiol., 79, 496, 10.1152/jn.1998.79.1.496

Messaoudi, 2002, BDNF triggers transcription-dependent, late phase LTP in vivo., J. Neurosci., 22, 7453, 10.1523/JNEUROSCI.22-17-07453.2002

10.1073/pnas.90.19.8802

10.1016/S0896-6273(00)80853-3

10.1073/pnas.90.14.6439

Mizuno, 2000, Involvement of brain-derived neurotrophic factor in spatial memory formation and maintenance in a radial arm maze test in rats., J. Neurosci., 20, 7116, 10.1523/JNEUROSCI.20-18-07116.2000

10.1002/(SICI)1097-4547(19980215)51:4<463::AID-JNR6>3.0.CO;2-A

10.1073/pnas.91.26.12673

10.1002/(SICI)1096-9861(19970414)380:3<373::AID-CNE6>3.0.CO;2-#

10.1016/S0006-8993(99)01592-9

10.1016/S0301-0082(00)00014-9

10.1016/S0169-328X(00)00054-1

10.1111/j.1460-9568.1995.tb01148.x

10.1038/373109a0

10.1016/0006-8993(96)00273-9

10.1126/science.8066450

Nibuya, 1995, Regulation of BDNF and trkB mRNA in rat brain by chronic electroconvulsive seizure and antidepressant drug treatments., J. Neurosci., 15, 7539, 10.1523/JNEUROSCI.15-11-07539.1995

10.1038/379826a0

Obermeier, 1994, Neuronal differentiation signals are controlled by nerve growth factor receptor/Trk binding sites for SHC and PLC γ., EMBO J., 13, 1585, 10.1002/j.1460-2075.1994.tb06421.x

Okabe, 1998, Hippocampal synaptic plasticity in mice overexpressing an embryonic subunit of the NMDA receptor., J. Neurosci., 18, 4177, 10.1523/JNEUROSCI.18-11-04177.1998

10.1016/S0169-328X(98)00222-8

10.1016/0896-6273(92)90067-N

10.1016/S0896-6273(00)80140-3

Pelleymounter, 1996, The effects of intrahippocampal BDNF and NGF on spatial learning in aged Long Evans rats., Mol. Chem. Neuropathol., 29, 211, 10.1007/BF02815003

Pollock, 2001, Effects of early visual experience and diurnal rhythms on BDNF mRNA and protein levels in the visual system, hippocampus, and cerebellum., J. Neurosci., 21, 3923, 10.1523/JNEUROSCI.21-11-03923.2001

10.1038/35049004

Pozzo-Miller, 1999, Impairments in high-frequency transmission, synaptic vesicle docking, and synaptic protein distribution in the hippocampus of BDNF knockout mice., J. Neurosci., 19, 4972, 10.1523/JNEUROSCI.19-12-04972.1999

10.1016/S0896-6273(00)80620-0

Qiao, 1998, Cerebellar brain-derived neurotrophic factor-TrkB defect associated with impairment of eyeblink conditioning in Stargazer mutant mice., J. Neurosci., 18, 6990, 10.1523/JNEUROSCI.18-17-06990.1998

10.1016/S0306-4522(00)00349-3

10.1002/1098-2396(200010)38:1<102::AID-SYN11>3.0.CO;2-K

10.1016/S0006-8993(97)01052-4

10.1016/S0006-8993(98)01010-5

10.1016/S0166-2236(00)01672-6

10.1146/annurev.ne.19.030196.002335

Shimada, 1998, TrkB signaling modulates spine density and morphology independent of dendrite structure in cultured neonatal Purkinje cells., J. Neurosci., 18, 8559, 10.1523/JNEUROSCI.18-21-08559.1998

10.1126/science.1321493

Smith, 1997, Anterograde transport of endogenous brain-derived neurotrophic factor in hippocampal mossy fibers., Neuroreport, 8, 1829, 10.1097/00001756-199705260-00008

10.1016/S0006-8993(98)00474-0

10.1016/0896-6273(94)90223-2

10.1073/pnas.94.15.8191

10.1046/j.1471-4159.2001.00054.x

Tanzi, 1893, I fatti e le induzioni nell'odierna isologia del sistema nervosa., Revista Sperimentale di Freniatria e di Medicina Legale, 19, 419

10.1016/S0896-6273(01)00561-X

10.1016/S0079-6123(00)28016-3

10.1016/0896-6273(93)90335-O

10.1038/80655

10.1038/46574

10.1101/lm.3.2-3.218

10.1016/S0092-8674(00)81826-7

10.1016/S0092-8674(00)81827-9

Tyler, 2001, BDNF enhances quantal neurotransmitter release and increases the number of docked vesicles at the active zones of hippocampal excitatory synapses., J. Neurosci., 21, 4249, 10.1523/JNEUROSCI.21-12-04249.2001

Tyler, W.J., Perrett, S., and Pozzo-Miller, L.D. 2002. The role of neurotrophins in neurotransmitter release. Neuroscientist (in press)..

Vaidya, 1997, 5-HT2A receptor-mediated regulation of brain-derived neurotrophic factor mRNA in the hippocampus and the neocortex., J. Neurosci., 17, 2785, 10.1523/JNEUROSCI.17-08-02785.1997

10.1016/S0304-3940(99)00006-3

10.1016/S0891-0618(00)00051-X

10.1002/(SICI)1097-4547(19991001)58:1<96::AID-JNR10>3.0.CO;2-N

10.1038/369233a0

10.1016/S0168-0102(99)00051-6

10.1017/S0958067000020959

10.1046/j.1460-9568.1999.00567.x

10.1016/S0306-4522(96)00613-6

Ying, 2002, Brain-derived neurotrophic factor induces long-term potentiation in intact adult hippocampus: Requirement for ERK activation coupled to CREB and upregulation of Arc synthesis., J. Neurosci., 22, 1532, 10.1523/JNEUROSCI.22-05-01532.2002

10.1146/annurev.neuro.24.1.1071

Zafra, 1990, Activity dependent regulation of BDNF and NGF mRNAs in the rat hippocampus is mediated by non-NMDA glutamate receptors., EMBO J., 9, 3545, 10.1002/j.1460-2075.1990.tb07564.x

10.1073/pnas.88.22.10037