Synapse elimination accompanies functional plasticity in hippocampal neurons

Proceedings of the National Academy of Sciences of the United States of America

Volumn 105, Issue 8, 2008, Pages 3123-3127

  Bastrikova, Natalia ^a   Gardner, Gregory A ^a   Reece, Jeff M ^a,c   Jeromin, Andreas ^b   Dudek, Serena M ^a  

^a NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^b ALLEN INSTITUTE FOR BRAIN SCIENCE   (United States)

^c Reecent Technologies LLC   (United States)

Author keywords

Cortex; Critical period; Development; Long term depression; Schizophrenia

Indexed keywords

GREEN FLUORESCENT PROTEIN; RED FLUORESCENT PROTEIN;

ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; BRAIN SLICE; CELL LABELING; DENDRITIC SPINE; ELECTROPHYSIOLOGY; GENE FUNCTION; HIPPOCAMPUS; IMAGING; LONG TERM DEPRESSION; MICROARRAY ANALYSIS; MICROELECTRODE; MOLECULAR DYNAMICS; NERVE CELL PLASTICITY; NONHUMAN; POSTSYNAPTIC POTENTIAL; PRESYNAPTIC NERVE; PRIORITY JOURNAL; RAT; SYNAPTIC INHIBITION; TISSUE CULTURE; ANIMAL; COMPARATIVE STUDY; CYTOLOGY; ELECTROSTIMULATION; IMAGE PROCESSING; NERVE CELL; NONPARAMETRIC TEST; PHYSIOLOGY; SPRAGUE DAWLEY RAT; SYNAPSE;

RATTUS;

ANIMALS; ELECTRIC STIMULATION; ELECTROPHYSIOLOGY; HIPPOCAMPUS; IMAGE PROCESSING, COMPUTER-ASSISTED; NEURONAL PLASTICITY; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; STATISTICS, NONPARAMETRIC; SYNAPSES;

EID: 42949176249     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0800027105     Document Type: Article

References (44)

1. Hua JY, Smith SJ (2004) Neural activity and the dynamics of central nervous system development. Nat Neurosci 7:327-332.
2. Hubel DH, Wiesel TN, LeVay S (1977) Plasticity of ocular dominance columns in monkey striate cortex. Philos Trans R Soc London B Biol Sci 278:377-409.
3. Stryker MP, Harris WA (1986) Binocular impulse blockade prevents the formation of ocular dominance columns in cat visual cortex. J Neurosci 6:2117-2133.
4. Reiter HO, Waitzman DM, Stryker MP (1986) Cortical activity blockade prevents ocular dominance plasticity in the kitten visual cortex. Exp Brain Res 65:182-188.
5. Kleinschmidt A, Bear MF, Singer W (1987) Blockade of "NMDA" receptors disrupts experience-dependent plasticity of kitten striate cortex. Science 238:355-358.
6. Bear MF, Kleinschmidt A, Gu QA, Singer W (1990) Disruption of experience-dependent synaptic modifications in striate cortex by infusion of an NMDA receptor antagonist. J Neurosci 10:909-925.
7. Colonnese MT, Constantine-Paton M (2006) Developmental period for N-methyl-D-aspartate (NMDA) receptor-dependent synapse elimination correlated with visuotopic map refinement. J Comp Neurol 494:738-751.
8. Lichtman JW, Colman H (2000) Synapse elimination and indelible memory. Neuron 25:269-278.
9. Antonini A, Stryker MP (1993) Rapid remodeling of axonal arbors in the visual cortex. Science 260:1819-1821.
10. Constantine-Paton M, Cline HT, Debski E (1990) Patterned activity, synaptic convergence, and the NMDA receptor in developing visual pathways. Annu Rev Neurosci 13:129-154.
11. Bear MF, Cooper LN, Ebner FF (1987) A physiological basis for a theory of synapse modification. Science 237:42-48.
12. Bienenstock EL, Cooper LN, Munro PW (1982) Theory for the development of neuron selectivity: Orientation specificity and binocular interaction in visual cortex. J Neurosci 2:32-48.
13. Dudek SM, Bear MF (1992) Homosynaptic long-term depression in area CA1 of hippocampus and effects of N-methyl-D-aspartate receptor blockade. Proc Natl Acad Sci USA 89:4363-4367.
14. Heynen AJ, et al. (2003) Molecular mechanism for loss of visual cortical responsiveness following brief monocular deprivation. Nat Neurosci 6:854-864.
15. Globus A, Scheibel AB (1967) The effect of visual deprivation on cortical neurons: a Golgi study. Exp Neurol 19:331-345.
16. Engert F, Bonhoeffer T (1999) Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature 399:66-70.
17. Knott GW, Holtmaat A, Wilbrecht L, Welker E, Svoboda K (2006) Spine growth precedes synapse formation in the adult neocortex in vivo. Nat Neurosci 9:1117-1124.
18. Matsuzaki M, Honkura N, Ellis-Davies GC, Kasai H (2004) Structural basis of long-term potentiation in single dendritic spines. Nature 429:761-766.
19. Nagerl UV, Eberhorn N, Chambridge SB, Bonhoeffer T (2004) Bidirectional activity-dependent morphological plasticity in hippocampal neurons. Neuron 44:759-767.
20. Fujii S, Saito K, Miyakawa H, Ito K, Kato H (1991) Reversal of long-term potentiation (depotentiation) induced by tetanus stimulation of the input to CA1 neurons of guinea pig hippocampal slices. Brain Res 555:112-122.
21. Dudek SM, Bear MF (1993) Bidirectional long-term modification of synaptic effectiveness in the adult and immature hippocampus. J Neurosci 13:2910-2918.
22. Mulkey RM, Herron CE, Malenka RC (1993) An essential role for protein phosphatases in hippocampal long-term depression. Science 261:1051-1055.
23. Barrionuevo G, Schottler F, Lynch G (1980) The effects of repetitive low frequency stimulation on control and "potentiated" synaptic responses in the hippocampus. Life Sci 27:2385-2391.
24. Lee HK, Barbarosie M, Kameyama K, Bear MF, Huganir RL (2000) Regulation of distinct AMPA receptor phosphorylation sites during bidirectional synaptic plasticity. Nature 405:955-959.
25. Zhou Q, Homma KJ, Poo MM (2004) Shrinkage of dendritic spines associated with long-term depression of hippocampal synapses. Neuron 44:749-757.
26. Umeda T, Ebihara T, Okabe S (2005) Simultaneous observation of stably associated presynaptic varicosities and postsynaptic spines: Morphological alterations of CA3-CA1 synapses in hippocampal slice cultures. Mol Cell Neurosci 28:264-274.
27. De Simoni A, Edwards FA (2006) Pathway specificity of dendritic spine morphology in identified synapses onto rat hippocampal CA1 neurons in organotypic slices. Hippocampus 16:1111-1124.
28. Baude A, Nusser Z, Molnar E, McIlhinney RA, Somogyi P (1995) High-resolution immunogold localization of AMPA type glutamate receptor subunits at synaptic and nonsynaptic sites in rat hippocampus. Neurosci 69:1031-1055.
29. Nusser Z, et al. (1998) Cell type and pathway dependence of synaptic AMPA receptor number and variability in the hippocampus. Neuron 21:545-559.
30. Wang XB, Yang Y, Zhou Q (2007) Independent expression of synaptic and morphological plasticity associated with long-term depression. J Neurosci 27:12419-12429.
31. Liu Y, Fields RD, Fitzgerald S, Festoff BW, Nelson PG (1994) Proteolytic activity, synapse elimination, and the Hebb synapse. J Neurobiol 25:325-335.
32. Bougeois JP, Rakic P (1993) Changes of synaptic density in the primary visual cortex of the macaque monkey from fetal to adult stage. J Neurosci 13:2801-2820.
33. Cajal SR (1893) Neue Darstellung vom histologischen bau des centralnervensystems. Anatomische Abtheilung des Arch fur Anat und Physiol, 319-428.
34. Harris KM, Jensen FE, Tsao B (1992) Three-dimensional structure of dendritic spines and synapses in rat hippocampus (CA1) at postnatal day 15 and adult ages: Implications for the maturation of synaptic physiology and long-term potentiation. J Neurosci 12:2685-2705.
35. Araya R, Jiang J, Eisenthal KB, Yuste R (2006) The spine neck filters membrane potentials. Proc Natl Acad Sci USA 103:17961-17966.
36. Bloodgood BL, Sabatini BL (2005) Neuronal activity regulates diffusion across the neck of dendritic spines. Science 310:866-869.
37. Kaufmann WE, Moser HW (2000) Dendritic anomalies in disorders associated with mental retardation. Cereb Cortex 10:981-991.
38. Glantz LA, Lewis DA (2000) Decreased dendritic spine density on prefrontal cortical pyramidal neurons in schizophrenia. Arch Gen Psychiatry 57:65-73.
39. Gray EG (1959) Axosomatic and axodendritic synapses of the cerebral cortex: An electron microscopic study. J Anat 83:420-433.
40. Konur S, Yuste R (2004) Imaging the motility of dendritic protrusions and axon terminals: Roles in axon sampling and synaptic competition. Mol Cell Neurosci 27:427-440.
41. Arellano JI, Espinosa A, Fairen A, Yuste R, DeFelipe J (2007) Non-synaptic dendritic spines in neocortex. Neuroscience 145:464-469.
42. Crozier RA, Wang Y, Liu CH, Bear MF (2007) Deprivation-induced synaptic depression by distinct mechanisms in different layers of mouse visual cortex. Proc Natl Acad Sci USA 104:1383-1388.
43. Shaner NC, et al. (2004) Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat Biotechnol 22:1567-1572.
44. Jeromin A, Yuan LL, Frick A, Pfaffinger P, Johnston D (2003) A modified Sindbis vector for prolonged gene expression in neurons. J Neurophysiol 90:2741-2745.