Synaptic plasticity in cortical systems

Current Opinion in Neurobiology

Volumn 9, Issue 2, 1999, Pages 203-208

  Klintsova, Anna Y ^a   Greenough, William T ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; HORMONE; NEUROTROPHIN; PROTEIN; RECEPTOR;

BRAIN CORTEX; LEARNING; LONG TERM POTENTIATION; MEMORY CONSOLIDATION; NERVE CELL PLASTICITY; PRIORITY JOURNAL; PROTEIN SYNTHESIS; REVIEW; SYNAPTOGENESIS;

EID: 0032927940     PISSN: 09594388     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-4388(99)80028-2     Document Type: Article

References (79)

1. Rosenzweig M.R., Bennett E.L., Diamond M.C. Chemical and anatomical plasticity of brain: replications and extentions. Gaito J. Macromolecules and Behavior. 1972;205-278 Appleton-Century-Croits, New York.
2. Volkmar F.R., Greenough W.T. Rearing complexity affects branching of dendrites in the visual cortex of the rat. Science. 176:1972;1445-1447.
3. Turner A.M., Greenough W.T. Differential rearing effects on rat visual cortex synapses. I. Synaptic and neuronal density and synapses per neuron. Brain Res. 329:1985;195-203.
4. Chang F.-L.F., Greenough W.T. Lateralized effects of monocular training on dendritic branching in adult split-brain rats. Brain Res. 232:1982;283-292.
5. Greenough W.T., Larson J., Withers G. Effects of unilateral and bilateral training in a reaching task on dendritic branching of neurons in the rat motor-sensory forelimb cortex. Behav Neural Biol. 44:1985;301-314.
6. Stewart M.G. Changes in dendritic and synaptic structure in chick forebrain consequent on passive avoidance conditioning. Andrew R.J. Neural and Behavioral Plasticity: The Use of the Domestic Chick as a Model. 1991;305-328 Oxford University Press, Oxford.
7. Stewart M.G., Rusakov D.A. Morphological changes associated with stages of memory formation in the chick following passive avoidance training. Behav Brain Res. 66:1995;21-28.
8. Kolb B., Whishaw I.Q. Plasticity in the neocortex: mechanisms underlying recovery from early brain damage. Prog Neurobiol. 32:1989;235-276.
9. Jones T.A., Schallert T. Use-dependent growth of pyramidal neurons after neocortical damage. J Neurosci. 14:1994;2140-2152.
10. Schallert T., Kozlowski D.A., Humm J.L., Cocke R.R. Use-dependent structural events in recovery of function. Adv Neurol. 73:1997;229-238.
11. Jones T.A., Kleim J.A., Greenough W.T. Synaptogenesis and dendritic growth in the cortex opposite unilateral sensorimotor cortex damage in adult rats: a quantitative electron microscopic examination. Brain Res. 733:1996;142-148.
12. Black J.E., Isaacs K.R., Anderson B.J., Alcantara A.A., Greenough W.T. Learning causes synaptogenesis, whereas motor activity causes angiogenesis, in cerebellar cortex of adult rats. Proc Natl Acad Sci USA. 87:1990;5568-5572.
13. Kleim J.A., Lussnig E., Schwarz E.R., Comery T.A., Greenough W.T. Synaptogenesis and Fos expression in the motor cortex of the adult rat following motor skill learning. J Neurosci. 16:1996;4529-4535.
14. Anderson B.J., Alcantara A.A., Greenough W.T. Motor skill learning: changes in synaptic organization of the rat cerebellar cortex. Neurobiol Learn Mem. 66:1996;221-229.
15. Kleim J.A., Swain R.A., Czerlanis C.M., Kelly J.L., Pipitone M.A., Greenough W.T. Learning-dependent dendritic hypertrophy of cerebellar stellate cells: plasticity of local circuit neurons. Neurobiol Learn Mem. 67:1997;29-33. Reports that dendrites of rat cerebellar inhibitory interneurons exhibit morphological plasticity in response to learning. Thus, experience-dependent adaptations in neuronal morphology are not unique to the primary input/output neurons but also occur in local circuit neurons.
16. Kleim J.A., Swain R.A., Armstrong K.E., Napper R.M.A., Jones T.A., Greenough W.T. Selective synaptic plasticity within the cerebellar cortex following complex motor skill learning. Neurobiol Learn Mem. 69:1998;274-289. In rats, cerebellar morphological plasticity in response to motor skill learning is largely confined to parallel fiber synapses. (See also Anderson et al. [14].) Given the previous reports that the majority of Purkinje cell activity is driven by parallel fiber activity, these findings are consonant with the view that addition of parallel fiber synapses would most dramatically affect Purkinje cell function.
17. Kleim J.A., Pipitone M.A., Czerlanis C.M., Greenough W.T. Structural stability within the lateral cerebellar nucleus of the rat following complex motor learning. Neurobiol Learn Mem. 69:1998;290-306. Important demonstration that the outputs remain morphologically stable in Purkinje cells whose inputs exhibit experience-induced plasticity. Both Purkinje cell axon synapses and extracerebellar synapses within one of the deep cerebellar nuclei were unaffected by acrobatic training or motor activity in terms of their number or the length of postsynaptic densities. These findings suggest that the lateral cerebellar nucleus may serve as a structurally stable output relay.
18. Kleim J.A., Vij K., Ballard D.H., Greenough W.T. Learning dependent synaptic modifications in the cerebellar cortex of the adult rat persist for at least four weeks. J Neurosci. 17:1997;717-721. This paper reports that both learned motor skills and the increase in synapse number presumed to support this learning persist in cerebellar cortex for a month in the absence of continued training.
19. Black J.E., Jones T.A., Nelson C.A., Greenough W.T. Neuronal plasticity and the developing brain. Alessi N., Coyle J.T., Harrison S.I., Eth S. The Handbook of Child and Adolescent Psychiatry, vol 6. 1998;34-53 John Wiley & Sons, New York. This chapter reviews mechanisms of plasticity in the developing and adult brain with respect to their function in behavior and competence. The possible human clinical significance of the animal findings is discussed.
20. Moser M.-B., Trommald M., Egeland T., Andersen P. Spatial training in a complex environment and isolation alter the spine distribution differently in rat CA1 pyramidal cells. J Comp Neurol. 380:1997;373-381.
21. Comery T.A., Stamoudis C.X., Irwin S.A., Greenough W.T. Increased density of multiple-head dendritic spines on medium-sized spiny neurons of the striatum in rats reared in a complex environment. Neurobiol Learn Mem. 66:1996;93-96.
22. Andersen P., Soleng A.F. Long-term potentiation and spatial training are both associated with the generation of new excitatory synapses. Brain Res Rev. 26:1998;353-359. This mini-review argues that synaptogenesis and synaptic morphology change in the adult rat hippocampus in associasion with LTP and spatial training.
23. Jones T.A., Klintsova A.Y., Kilman V.L., Sirevaag A.M., Greenough W.T. Induction of multiple synapses by experience in the visual cortex of adult rats. Neurobiol Learn Mem. 68:1997;13-20. Prototypical example of several recent reports of multiple utilization of synaptic components (multiple postsynaptic elements in this case) as an aspect of synaptogenesis in response to experience.
24. Kolb B., Cote S., Ribeiro-da-Silva A., Cuello A.C. NGF stimulates recovery of function and dendritic growth after unilateral motor cortex lesions in rats. Neuroscience. 76:1997;1139-1151.
25. Kolb B., Stewart J., Sutherland R.J. Recovery of function is associated with increased spine density in cortical pyramidal cells after frontal lesions or noradrenaline depletion in neonatal rats. Behav Brain Res. 89:1997;61-70.
26. Rowntree S., Kolb B. Antibodies to bFGF block functional recovery and dendritic compensation after motor cortex lesions. Eur J Neurosci. 9:1997;2432-2442.
27. Lindsay R.M. Neurotrophins and receptors. Prog Brain Res. 103:1994;3-14.
28. Lewin G.R., Barde Y.-A. Physiology of neurotrophins. Annu Rev Neurosci. 19:1996;289-317.
29. Skaper S.D., Walsh F.S. Neurotrophic molecules: strategies for designing effective therapeutic molecules in neurodegeneration. Mol Cell Neurosci. 12:1998;179-193.
30. Morrison M.E., Mason C.A. Granule neuron regulation of Purkinje cell development: striking a balance between neurotrophin and glutamate signaling. J Neurosci. 18:1998;3563-3573.
31. Shimada A., Mason C.A., Morrison M.E. TrkB signaling modulates spine density and morphology independent of dendrite structure in cultured neonatal Purkinje cells. J Neurosci. 18:1998;8559-8570.
32. Martinez A., Alcantara S., Borrell V., Del Rio J.A., Blasi J., Otal R., Campos N., Boronat A., Barbacid M., Silos-Santiago I., Soriano E. TrkB and TrkC signaling are required for maturation and synaptogenesis of hippocampal connections. J Neurosci. 18:1998;7336-7350.
33. Vicario-Abejon C., Collin C., McKay R.D.G., Segal M. Neurotrophins induce formation of functional excitatory and inhibitory synapses between cultured hippocampal neurons. J Neurosci. 18:1998;7256-7271. This paper demonstrates the distinct and specific role of neurotrophins (BDNF and NT-3) in the formation of synapses and axonal branching in the hippocampus. The authors report a sevenfold (!) increase in the number of functional connections in hippocampal neuron cultures after neurotrophin treatment. Interestingly, BDNF induced formation of both excitatory and inhibitory synapses, whereas NT-3 addition resulted in formation of only excitatory synapses. In addition, both BDNF and NT-3 increased dendritic complexity of neurons in culture, but only BDNF stimulated growth of axons.
34. Lo D.C. Neurotrophic factors and synaptic plasticity. Neuron. 15:1995;979-981.
35. Thoenen H. Neurotrophins and neuronal plasticity. Science. 270:1995;593-598.
36. Bonhoeffer T. Neurotrophins and activity-dependent development of the neocortex. Curr Opin Neurobiol. 6:1996;119-126.
37. Berninger B., Poo M.-m. Fast actions of neurotrophic factors. Curr Opin Neurobiol. 6:1996;324-330.
38. Patterson S.L., Abel T., Deuel T.A.S., Martin K.C., Rose J.C., Kandel E.R. Recombinant BDNF rescues deficits in basal synaptic transmission and hippocampal LTP in BDNF knockout mice. Neuron. 16:1996;1137-1145.
39. Kang H., Welcher A.A., Shelton D., Schuman E.M. Neurotrophins and time: different roles for TrkB signalling in hippocampal long-term potentiation. Neuron. 19:1997;653-664. The BDNF-TrkB signalling pathway does not appear to be necessary for LTP induced by all protocols: in the rat hippocampi, LTP induced by four trains of 100 Hz tetani does not require functioning TrkB receptors either for induction or during the maintenance phase. LTP induced by theta-burst or low-frequency protocols decayed if BDNF receptors were blocked.
40. Akaneya Y., Tsumoto T., Kinoshita S., Hatanaka H. Brain-derived neurotrophic factor enhances long-term potentiation in rat visual cortex. J Neurosci. 17:1997;6707-6716.
41. Figurov A., Pozzo-Miller L.D., Olafsson P., Wang T., Lu B. Regulation of synaptic responses to high-frequency stimulation and LTP by neurotrophins in the hippocampus. Nature. 381:1996;706-709.
42. Korte M., Carroll P., Wolf E., Brem G., Thoenen H., Bonhoeffer T. Hippocampal long-term potentiation is impaired in mice lacking brain-derived neurotrophic factor. Proc Natl Acad Sci USA. 92:1995;8856-8860.
43. McAllister A.K., Katz L.C., Lo D.C. Opposing roles for endogenous BDNF and NT-3 in regulating cortical dendritic growth. Neuron. 18:1997;767-778. Endogenous neurotrophins are necessary for regulating dendritic growth of pyramidal neurons in developing ferret visual cortex. This paper provides evidence of opposing regulation of dendritic outgrowth and retraction in pyramidal neurons by BDNF and NT-3 in layers IV and VI of visual cortex. The authors call this bidirectional dendrite growth/pruning regulation a 'push-pull system'. These findings add to the growing evidence for distinct actions of different neurotrophins on neuronal growth and patterns of contact formation.
44. Cohen-Cory S., Fraser S.E. Effects of brain-derived neurotrophic factor on optic axon branching and remodelling in vivo. Nature. 378:1995;192-195.
45. Cabelli R.J., Shelton D.L., Segal R.A., Shatz C.J. Blockade of endogenous ligands of TrkB inhibits formation of ocular dominance columns. Neuron. 19:1997;63-76. This is one of a few in vivo studies of the effect of endogenous neurotrophins on neuronal morphology and connectivity. This paper demonstrates that the presence of limited amounts of endogenous ligands of trkB - BDNF and NT-4/5 - is required for formation of ocular dominance columns in the visual cortex of cats. Infused excess of trkB-IgG, but not trkA-IgG or trkC-IgG, prevents the formation of ocular dominance patches.
46. Riddle D.R., Lo D.C., Katz L.C. NT-4-mediated rescue of lateral geniculate neurons from effects of monocular deprivation. Nature. 378:1995;189-191.
47. Narisawa-Saito M., Carnahan J., Araki K., Yamaguchi T., Nawa H. Brain-derived neurotrophic factor regulates the expression of AMPA receptor proteins in neocortical neurons. Neuroscience. 88:1999;1009-1014.
48. Malgaroli A. Silent synapses: I can't hear you! Could you please speak aloud? Nat Neurosci. 2:1999;3-5.
49. Tong G., Malenka R.C., Nicoll R.A. Long-term potentiation in cultures of single hippocampal granule cells: a presynaptic form of plasticity. Neuron. 16:1996;1147-1157.
50. Kimura F., Otsu Y., Tsumoto T. Presynaptically silent synapses: spontaneously active terminals without stimulus-evoked release demonstrated in cortical autapses. J Neurophysiol. 77:1997;2805-2815.
51. Isaac J.T.R., Nicoll R.A., Malenka R.C. Evidence for silent synapses: implications for the expression of LTP. Neuron. 15:1995;427-434.
52. Isaac J.T.R., Crair M.C., Nicoll R.A., Malenka R.C. Silent synapses during development of thalamocortical inputs. Neuron. 18:1997;269-280. This paper provides direct (by attempts to induce LTP) evidence that functionally silent synapses exist in thalamocortical connections at postnatal day 2-5 in rat whisker barrels. They disappear by postnatal day 8-9, paralleling the loss of susceptibility of these synapses to LTP. It remains unclear whether all newly formed synapses initially contain only NMDA receptors or there is an intermix of functional and silent synapses.
53. Liao D., Hessler N.A., Malinow R. Activation of postsynaptically silent synapses during pairing-induced LTP in CA1 region of hippocampal slice. Nature. 375:1995;400-404.
54. Liao D., Zhang X., O'Brian R., Ehlers M.D., Huganir R.L. Regulation of morphological postsynaptic silent synapses in developing hippocampal neurons. Nat Neurosci. 2:1999;37-43. This is the first attempt to visualize silent synapses by using immunocytochemical double labeling of AMPA and NMDA receptors in synapses of developing rat hippocampal neurons. A possible morphological correlate of silent synapses is characterized: gradual addition of AMPA receptors to synapses during development is reported. The data also suggests that the regulation of AMPA receptors occurs at a very local level (based on the dramatically different levels of AMPA receptors in adjacent spines).
55. Durand G.M., Kovalchuk Y., Konnert A. Long-term potentiation and functional synapse induction in developing hippocampus. Nature. 381:1996;71-75.
56. Rumpel S., Hatt H., Gottmann K. Silent synapses in the developing rat visual cortex: evidence for postsynaptic expression of synaptic plasticity. J Neurosci. 18:1998;8863-8874. These data support a postsynaptic mechanism underlying silent synapses. The data presented suggest that silent synapses do not contain functional AMPA receptors. An activity-dependent mechanism of silent synapse conversion into functional synapses is proposed, via either modification of previously nonfunctional AMPA receptors or membrane insertion of AMPA receptors.
57. Gomperts S.N., Rao A., Craig A.M., Malenka R.C., Nicoll R.A. Postsynaptically silent synapses in single neuron cultures. Neuron. 21:1998;1443-1451.
58. Nusser Z., Lujan R., Laube G., Roberts J.D.B., Molnar E., Somogyi P. Cell type and pathway dependence of synaptic AMPA receptor number and variability in the hippocampus. Neuron. 21:1998;545-559.
59. Petralia R.S., Esteban J.A., Wang Y.-X., Partridge J.G., Zhao H.-M., Wenthold R.J., Malinow R. Selective acquisition of AMPA receptors over postnatal development suggests a molecular basis for silent synapses. Nat Neurosci. 2:1999;31-36. Post-embedding immunogold electron microscopy was used to examine NMDA and AMPA receptors during the postnatal development of rat hippocampus. Direct evidence that AMPA receptor numbers increase per synapse during development is provided, whereas the number of NMDA receptors per synapse remains stable.
60. Crair M.C., Malenka R.C. A critical period for long-term potentiation at thalamocortical synapses. Nature. 375:1995;325-328.
61. Nayak A., Zastrow D.J., Lickteig R., Zahniser N.R., Browning M.D. Maintenance of late-phase LTP is accompanied by PKA-dependent increase in AMPA receptor synthesis. Nature. 394:1998;680-683.
62. Warren S.G., Humphreys A.G., Juraska J.M., Greenough W.T. LTP varies across the estrous cycle: enhanced synaptic plasticity in proestrus rats. Brain Res. 703:1995;26-30.
63. Woolley C.S. Estrogen-mediated structural and functional synaptic plasticity in the female rat hippocampus. Horm Behav. 34:1998;140-148.
64. Murphy D.D., Segal M. Regulation of dendritic spine density in cultured rat hippocampal neurons by steroid hormones. J Neurosci. 16:1996;4059-4068.
65. Murphy D.D., Cole N.B., Greenberger V., Segal M. Estradiol increases dendritic spine density by reducing GABA neurotransmission in hippocampal neurons. J Neurosci. 18:1998;2550-2559.
66. Lee K.S., Schottler F., Oliver M., Lynch G. Brief bursts of high-frequency stimulation produce two types of structural change in rat hippocampus. J Neurophysiol. 44:1980;247-258.
67. Hosokawa T., Rusakov D.A., Bliss T.V.P., Fine A. Repeated confocal imaging of individual dendritic spines in the living hippocampal slice: evidence for changes in length and orientation associated with chemically induced LTP. J Neurosci. 15:1995;5560-5573.
68. Geinisman Y., de Toledo-Morrell L., Morrell F., Heller R.E., Rossi M., Parshall R.F. Structural synaptic correlate of long-term potentiation: formation of axo-spinous synapses with multiple, completely partitioned transmission zones. Hippocampus. 3:1993;435-446.
69. Geinisman Y., de Toledo-Morrell L., Morrell F., Persina I.S., Beatty M.A. Synapse restructuring associated with the maintenance phase of hippocampal long-term potentiation. J Comp Neurol. 368:1996;413-423.
70. Geinisman Y., Disterhoft L.F., Gundersen H.J.G., McEchron M.D., Persina I.S., Power J.M., Van der Zee E.A., West M.J. Trace eyeblink conditioning induces a restructuring of preexisting synapses rather than synaptogenesis. Soc Neurosci Abstr. 24:1998;560.
71. Buchs P.A., Muller D. Induction of long-term potentiation is associated with major ultrastructural changes of activated synapses. Proc Natl Acad Sci USA. 93:1996;8040-8045.
72. Sorra K.E., Harris K.M. Stability in synapse number and size at 2 hr after long-term potentiation in hippocampal area CA1. J Neurosci. 18:1998;658-671. This study reports that LTP does not cause a net formation or enlargement of synapses at 2 h post-tetanus in hippocampal CA1. By default, it supports the hypothesis that LTP involves a redistribution of synaptic weights among existing synapses.
73. Steward O., Levy W.B. Preferential localization of polyribosomes under the base of dendritic spines in granule cells of the dentate gyrus. J Neurosci. 2:1982;284-291.
74. Weiler I.J., Greenough W.T. Potassium ion stimulation triggers protein translation in synaptoneurosomal polyribosomes. Mol Cell Neurosci. 2:1991;305-314.
75. Weiler I.J., Greenough W.T. Metabotropic glutamate receptors trigger postsynaptic protein synthesis. Proc Natl Acad Sci USA. 90:1993;7168-7171.
76. •] for synaptic protein synthesis.
77. •]).
78. Weiler I.J., Irwin S.A., Klintsova A.Y., Spencer C.M., Brazelton A.D., Miyashiro K., Comery T.A., Patel B., Eberwine J., Greenough W.T. Fragile-X mental retardation protein is translated near synapses in response to neurotransmitter activation. Proc Natl Acad Sci USA. 94:1997;5395-5400. The protein whose absence is associated with the leading cause of inherited mental retardation is translated at synapses in response to glutamate activation of metabotropic receptors. This is the first, and still the only, protein to be discovered to be translated at synapses in response to neurotransmitter.
79. •]). Spine structure and number abnormalities in a knockout mouse model of this syndrome are described. The synthesis of this protein at the synapse appears to be essential to normal synapse maturation and pruning.