Mossy Fiber-CA3 Synapses Mediate Homeostatic Plasticity in Mature Hippocampal Neurons

Neuron

Volumn 77, Issue 1, 2013, Pages 99-114

  Lee, Kea Joo ^a   Queenan, Bridget N ^a   Rozeboom, Aaron M ^a   Bellmore, Ryan ^a   Lim, Seung T ^a   Vicini, Stefano ^a   Pak, Daniel T S ^a  

^a GEORGETOWN UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

POLO LIKE KINASE 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ACTIVITY; CELL FUNCTION; CELL POPULATION; CELL STRUCTURE; CONTROLLED STUDY; ELECTROENCEPHALOGRAM; EMBRYO; ENZYME ACTIVITY; EXCITATORY POSTSYNAPTIC POTENTIAL; GRANULE CELL; HIPPOCAMPAL CA3 REGION; HOMEOSTASIS; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR DYNAMICS; MOSSY FIBER; MOUSE; NERVE CELL; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; RAT; SYNAPSE;

ANIMALS; CA3 REGION, HIPPOCAMPAL; CELLS, CULTURED; HIPPOCAMPUS; HOMEOSTASIS; MOSSY FIBERS, HIPPOCAMPAL; NEURONAL PLASTICITY; NEURONS; RATS; SYNAPSES;

EID: 84872175082     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2012.10.033     Document Type: Article

References (45)

1. Amaral D.G., Dent J.A. Development of the mossy fibers of the dentate gyrus: I. A light and electron microscopic study of the mossy fibers and their expansions. J. Comp. Neurol. 1981, 195:51-86.
2. Bekkers J.M., Stevens C.F. Cable properties of cultured hippocampal neurons determined from sucrose-evoked miniature EPSCs. J. Neurophysiol. 1996, 75:1250-1255.
3. Burrone J., O'Byrne M., Murthy V.N. Multiple forms of synaptic plasticity triggered by selective suppression of activity in individual neurons. Nature 2002, 420:414-418.
4. Carpenter-Hyland E.P., Chandler L.J. Homeostatic plasticity during alcohol exposure promotes enlargement of dendritic spines. Eur. J. Neurosci. 2006, 24:3496-3506.
5. Chicurel M.E., Harris K.M. Three-dimensional analysis of the structure and composition of CA3 branched dendritic spines and their synaptic relationships with mossy fiber boutons in the rat hippocampus. J. Comp. Neurol. 1992, 325:169-182.
6. Echegoyen J., Neu A., Graber K.D., Soltesz I. Homeostatic plasticity studied using in vivo hippocampal activity-blockade: synaptic scaling, intrinsic plasticity and age-dependence. PLoS ONE 2007, 2:e700.
7. Evers D.M., Matta J.A., Hoe H.S., Zarkowsky D., Lee S.H., Isaac J.T., Pak D.T. Plk2 attachment to NSF induces homeostatic removal of GluA2 during chronic overexcitation. Nat. Neurosci. 2010, 13:1199-1207.
8. Forti L., Bossi M., Bergamaschi A., Villa A., Malgaroli A. Loose-patch recordings of single quanta at individual hippocampal synapses. Nature 1997, 388:874-878.
9. Galimberti I., Gogolla N., Alberi S., Santos A.F., Muller D., Caroni P. Long-term rearrangements of hippocampal mossy fiber terminal connectivity in the adult regulated by experience. Neuron 2006, 50:749-763.
10. Goel A., Lee H.-K. Persistence of experience-induced homeostatic synaptic plasticity through adulthood in superficial layers of mouse visual cortex. J. Neurosci. 2007, 27:6692-6700.
11. Han E.B., Stevens C.F. Development regulates a switch between post- and presynaptic strengthening in response to activity deprivation. Proc. Natl. Acad. Sci. USA 2009, 106:10817-10822.
12. Hatanaka Y., Mukai H., Mitsuhashi K., Hojo Y., Murakami G., Komatsuzaki Y., Sato R., Kawato S. Androgen rapidly increases dendritic thorns of CA3 neurons in male rat hippocampus. Biochem. Biophys. Res. Commun. 2009, 381:728-732.
13. Henze D.A., Card J.P., Barrionuevo G., Ben-Ari Y., Lauri S.E., Segerstråle M., Vesikansa A., Maingret F., Mulle C., Collingridge L., et al. Large amplitude miniature excitatory postsynaptic currents in hippocampal CA3 pyramidal neurons are of mossy fiber origin. J. Neurophysiol. 1997, 77:1075-1086.
14. Ibata K., Sun Q., Turrigiano G.G. Rapid synaptic scaling induced by changes in postsynaptic firing. Neuron 2008, 57:819-826.
15. Jonas P., Major G., Sakmann B. Quantal components of unitary EPSCs at the mossy fibre synapse on CA3 pyramidal cells of rat hippocampus. J. Physiol. 1993, 472:615-663.
16. Kim J., Tsien R.W. Synapse-specific adaptations to inactivity in hippocampal circuits achieve homeostatic gain control while dampening network reverberation. Neuron 2008, 58:925-937.
17. Kolomeets N.S., Orlovskaya D.D., Uranova N.A. Decreased numerical density of CA3 hippocampal mossy fiber synapses in schizophrenia. Synapse 2007, 61:615-621.
18. Lee K.J., Lee Y., Rozeboom A., Lee J.-Y., Udagawa N., Hoe H.-S., Pak D.T.S. Requirement for Plk2 in orchestrated Ras and Rap signaling, homeostatic structural plasticity, and memory. Neuron 2011, 69:957-973.
19. Liu G., Tsien R.W. Properties of synaptic transmission at single hippocampal synaptic boutons. Nature 1995, 375:404-408.
20. Magee J.C., Cook E.P. Somatic EPSP amplitude is independent of synapse location in hippocampal pyramidal neurons. Nat. Neurosci. 2000, 3:895-903.
21. Malinow R., Malenka R.C. AMPA receptor trafficking and synaptic plasticity. Annu. Rev. Neurosci. 2002, 25:103-126.
22. Mellor J., Nicoll R.A. Hippocampal mossy fiber LTP is independent of postsynaptic calcium. Nat. Neurosci. 2001, 4:125-126.
23. Mitra A., Mitra S.S., Tsien R.W. Heterogeneous reallocation of presynaptic efficacy in recurrent excitatory circuits adapting to inactivity. Nat. Neurosci. 2012, 15:250-257.
24. Murthy V.N., Schikorski T., Stevens C.F., Zhu Y. Inactivity produces increases in neurotransmitter release and synapse size. Neuron 2001, 32:673-682.
25. O'Brien R.J., Kamboj S., Ehlers M.D., Rosen K.R., Fischbach G.D., Huganir R.L. Activity-dependent modulation of synaptic AMPA receptor accumulation. Neuron 1998, 21:1067-1078.
26. Pak D.T.S., Sheng M. Targeted protein degradation and synapse remodeling by an inducible protein kinase. Science 2003, 302:1368-1373.
27. Pozo K., Goda Y. Unraveling mechanisms of homeostatic synaptic plasticity. Neuron 2010, 66:337-351.
28. Ramon y Cajal S. Histologie du Système Nerveux de l'homme et des Vertébrés 1911, Maloine, Paris.
29. Reid C.A., Fabian-Fine R., Fine A. Postsynaptic calcium transients evoked by activation of individual hippocampal mossy fiber synapses. J. Neurosci. 2001, 21:2206-2214.
30. Reyes M., Stanton P.K. Induction of hippocampal long-term depression requires release of Ca2+ from separate presynaptic and postsynaptic intracellular stores. J. Neurosci. 1996, 16:5951-5960.
31. Seeburg D.P., Feliu-Mojer M., Gaiottino J., Pak D.T.S., Sheng M. Critical role of CDK5 and Polo-like kinase 2 in homeostatic synaptic plasticity during elevated activity. Neuron 2008, 58:571-583.
32. Singec I., Knoth R., Ditter M., Hagemeyer C.E., Rosenbrock H., Frotscher M., Volk B. Synaptic vesicle protein synaptoporin is differently expressed by subpopulations of mouse hippocampal neurons. J. Comp. Neurol. 2002, 452:139-153.
33. Stewart M.G., Davies H.A., Sandi C., Kraev I.V., Rogachevsky V.V., Peddie C.J., Rodriguez J.J., Cordero M.I., Donohue H.S., Gabbott P.L., Popov V.I. Stress suppresses and learning induces plasticity in CA3 of rat hippocampus: a three-dimensional ultrastructural study of thorny excrescences and their postsynaptic densities. Neuroscience 2005, 131:43-54.
34. Takai Y., Nakanishi H. Nectin and afadin: novel organizers of intercellular junctions. J. Cell Sci. 2003, 116:17-27.
35. Tauck D.L., Nadler J.V. Evidence of functional mossy fiber sprouting in hippocampal formation of kainic acid-treated rats. J. Neurosci. 1985, 5:1016-1022.
36. Thiagarajan T.C., Lindskog M., Tsien R.W. Adaptation to synaptic inactivity in hippocampal neurons. Neuron 2005, 47:725-737.
37. Treves A., Rolls E.T. Computational constraints suggest the need for two distinct input systems to the hippocampal CA3 network. Hippocampus 1992, 2:189-199.
38. Tsamis I.K., Mytilinaios G.D., Njau N.S., Fotiou F.D., Glaftsi S., Costa V., Baloyannis J.S. Properties of CA3 dendritic excrescences in Alzheimer's disease. Curr. Alzheimer Res. 2010, 7:84-90.
39. Turrigiano G.G. The self-tuning neuron: synaptic scaling of excitatory synapses. Cell 2008, 135:422-435.
40. Turrigiano G.G., Nelson S.B. Hebb and homeostasis in neuronal plasticity. Curr. Opin. Neurobiol. 2000, 10:358-364.
41. Turrigiano G.G., Leslie K.R., Desai N.S., Rutherford L.C., Nelson S.B. Activity-dependent scaling of quantal amplitude in neocortical neurons. Nature 1998, 391:892-896.
42. Wierenga C.J., Ibata K., Turrigiano G.G. Postsynaptic expression of homeostatic plasticity at neocortical synapses. J. Neurosci. 2005, 25:2895-2905.
43. Wierenga C.J., Walsh M.F., Turrigiano G.G. Temporal regulation of the expression locus of homeostatic plasticity. J. Neurophysiol. 2006, 96:2127-2133.
44. Williams M.E., Wilke S.A., Daggett A., Davis E., Otto S., Ravi D., Ripley B., Bushong E.A., Ellisman M.H., Klein G., Ghosh A. Cadherin-9 regulates synapse-specific differentiation in the developing hippocampus. Neuron 2011, 71:640-655.
45. Woodhams P.L., Webb M., Atkinson D.J., Seeley P.J. A monoclonal antibody, Py, distinguishes different classes of hippocampal neurons. J. Neurosci. 1989, 9:2170-2181.