Activity-dependent dendritic spine neck changes are correlated with synaptic strength

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

Volumn 111, Issue 28, 2014, Pages

  Araya, Roberto ^a,b   Vogels, Tim P ^a,c   Yuste, Rafael ^a  

^a Howard Hughes Medical Institute   (United States)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Basal dendrites; Neocortex; STDP

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN FUNCTION; BRAIN SLICE; CONTROLLED STUDY; DENDRITIC SPINE; ELECTROSTIMULATION; EVOKED RESPONSE; EXCITATORY POSTSYNAPTIC POTENTIAL; NERVE CELL PLASTICITY; NONHUMAN; POSTSYNAPTIC MEMBRANE; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; STRIATE CORTEX; SYNAPTIC EFFICACY; SYNAPTIC POTENTIAL; SYNAPTIC TRANSMISSION;

BASAL DENDRITES; NEOCORTEX; STDP;

ANIMALS; DENDRITES; FEMALE; HUMANS; MALE; MICE; NECK; PYRAMIDAL CELLS; SPINE; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 84904304923     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1321869111     Document Type: Article

References (63)

1. Ramón y Cajal S (1899) La Textura del Sistema Nerviosa del Hombre y los Vertebrados (Moya, Madrid).
2. Gray EG (1959) Electron microscopy of synaptic contacts on dendrite spines of the cerebral cortex. Nature 183(4675):1592-1593.
3. Colonnier M (1968) Synaptic patterns on different cell types in the different laminae of the cat visual cortex. An electron microscope study. Brain Res 9(2):268-287.
4. Arellano JI, Benavides-Piccione R, DeFelipe J, Yuste R (2007) Ultrastructure of dendritic spines: Correlation between synaptic and spine morphologies. Front Neurosci 1(1):131-143.
5. Arellano JI, Espinosa A, Fairén A, Yuste R, DeFelipe J (2007) Non-synaptic dendritic spines in neocortex. Neuroscience 145(2):464-469.
6. Harris KM (1999) Structure, development, and plasticity of dendritic spines. Curr Opin Neurobiol 9(3):343-348.
7. Chen JL, et al. (2012) Clustered dynamics of inhibitory synapses and dendritic spines in the adult neocortex. Neuron 74(2):361-373.
8. Shepherd GM (1996) The dendritic spine: Amultifunctional integrative unit. J Neurophysiol 75(6):2197-2210.
9. Yuste R (2010) Dendritic Spines (MIT Press, Cambridge, MA).
10. Harris KM, Kater SB (1994) Dendritic spines: Cellular specializations imparting both stability and flexibility to synaptic function. Annu Rev Neurosci 17:341-371.
11. Svoboda K, Tank DW, Denk W (1996) Direct measurement of coupling between dendritic spines and shafts. Science 272(5262):716-719.
12. Majewska A, Tashiro A, Yuste R (2000) Regulation of spine calcium dynamics by rapid spine motility. J Neurosci 20(22):8262-8268.
13. Bloodgood BL, Sabatini BL (2005) Neuronal activity regulates diffusion across the neck of dendritic spines. Science 310(5749):866-869.
14. Yuste R, Denk W (1995) Dendritic spines as basic functional units of neuronal integration. Nature 375(6533):682-684.
15. Denk W, Sugimori M, Llinás R (1995) Two types of calcium response limited to single spines in cerebellar Purkinje cells. Proc Natl Acad Sci USA 92(18):8279-8282.
16. Kovalchuk Y, Eilers J, Lisman J, Konnerth A (2000) NMDA receptor-mediated subthreshold Ca(2+) signals in spines of hippocampal neurons. J Neurosci 20(5):1791-1799.
17. Koester HJ, Sakmann B (1998) Calcium dynamics in single spines during coincident pre- and postsynaptic activity depend on relative timing of back-propagating action potentials and subthreshold excitatory postsynaptic potentials. Proc Natl Acad Sci USA 95(16):9596-9601.
18. Yuste R, Majewska A, Cash SS, Denk W (1999) Mechanisms of calcium influx into hippocampal spines: Heterogeneity among spines, coincidence detection by NMDA receptors, and optical quantal analysis. J Neurosci 19(6):1976-1987.
19. Holmes WR (1990) Is the function of dendritic spines to concentrate calcium? Brain Res 519(1-2):338-342.
20. Koch C, Zador A (1993) The function of dendritic spines: Devices subserving biochemical rather than electrical compartmentalization. J Neurosci 13(2):413-422.
21. Matsuzaki M, Honkura N, Ellis-Davies GC, Kasai H (2004) Structural basis of long-term potentiation in single dendritic spines. Nature 429(6993):761-766.
22. Chang HT (1952) Cortical neurons with particular reference to the apical dendrites. Cold Spring Harb Symp Quant Biol 17:189-202.
23. Rall W (1974) Dendritic spines, synaptic potency and neuronal plasticity. Cellular Mechanisms Subserving Changes in Neuronal Activity, eds Woody CD, et al. (Brain Information Services, Los Angeles), pp 13-21.
24. Jack JJB, Noble D, Tsien RW (1975) Electric Current Flow in Excitable Cells (Oxford Univ Press, London).
25. Llinás R, Hillman DE (1969) Physiological and morphological organization of the cerebellar circuits in various vertebrates. Neurobiology of Cerebellar Evolution and Development, ed Llinas R (American Medical Assoc Education and Research Foundation, Chicago), pp 43-73.
26. Koch C, Poggio T (1983) Electrical properties of dendritic spines. Trends Neurosci 6:80-83.
27. Miller JP, Rall W, Rinzel J (1985) Synaptic amplification by active membrane in dendritic spines. Brain Res 325(1-2):325-330.
28. Segev I, Rall W (1988) Computational study of an excitable dendritic spine. J Neurophysiol 60(2):499-523.
29. Tsay D, Yuste R (2004) On the electrical function of dendritic spines. Trends Neurosci 27(2):77-83.
30. Yuste R (2011) Dendritic spines and distributed circuits. Neuron 71(5):772-781.
31. Araya R, Jiang J, Eisenthal KB, Yuste R (2006) The spine neck filters membrane potentials. Proc Natl Acad Sci USA 103(47):17961-17966.
32. Harnett MT, Makara JK, Spruston N, Kath WL, Magee JC (2012) Synaptic amplification by dendritic spines enhances input cooperativity. Nature 491(7425):599-602.
33. Bloodgood BL, Giessel AJ, Sabatini BL (2009) Biphasic synaptic Ca influx arising from compartmentalized electrical signals in dendritic spines. PLoS Biol 7(9):e1000190.
34. Rose CR, Kovalchuk Y, Eilers J, Konnerth A (1999) Two-photon Na+ imaging in spines and fine dendrites of central neurons. Pflugers Arch 439(1-2):201-207.
35. Grunditz A, Holbro N, Tian L, Zuo Y, Oertner TG (2008) Spine neck plasticity controls postsynaptic calcium signals through electrical compartmentalization. J Neurosci 28(50):13457-13466.
36. Araya R, Nikolenko V, Eisenthal KB, Yuste R (2007) Sodium channels amplify spine potentials. Proc Natl Acad Sci USA 104(30):12347-12352.
37. Conti R, Lisman J (2003) The high variance of AMPA receptor- and NMDA receptor-mediated responses at single hippocampal synapses: Evidence for multiquantal release. Proc Natl Acad Sci USA 100(8):4885-4890.
38. Emptage N, Bliss TV, Fine A (1999) Single synaptic events evoke NMDA receptormediated release of calcium from internal stores in hippocampal dendritic spines. Neuron 22(1):115-124.
39. Enoki R, Hu YL, Hamilton D, Fine A (2009) Expression of long-term plasticity at individual synapses in hippocampus is graded, bidirectional, and mainly presynaptic: optical quantal analysis. Neuron 62(2):242-253.
40. Malinow R, Otmakhov N, Blum KI, Lisman J (1994) Visualizing hippocampal synaptic function by optical detection of Ca2+ entry through the N-methyl-D-aspartate channel. Proc Natl Acad Sci USA 91(17):8170-8174.
41. Oertner TG, Sabatini BL, Nimchinsky EA, Svoboda K (2002) Facilitation at single synapses probed with optical quantal analysis. Nat Neurosci 5(7):657-664.
42. Toni N, et al. (2007) Synapse formation on neurons born in the adult hippocampus. Nat Neurosci 10(6):727-734.
43. Kalisman N, Silberberg G, Markram H (2005) The neocortical microcircuit as a tabula rasa. Proc Natl Acad Sci USA 102(3):880-885.
44. Bolshakov VY, Siegelbaum SA (1995) Regulation of hippocampal transmitter release during development and long-term potentiation. Science 269(5231):1730-1734.
45. Losonczy A, Magee JC (2006) Integrative properties of radial oblique dendrites in hippocampal CA1 pyramidal neurons. Neuron 50(2):291-307.
46. Matsuzaki M, et al. (2001) Dendritic spine geometry is critical for AMPA receptor expression in hippocampal CA1 pyramidal neurons. Nat Neurosci 4(11):1086-1092.
47. Tanaka J, et al. (2008) Protein synthesis and neurotrophin-dependent structural plasticity of single dendritic spines. Science 319(5870):1683-1687.
48. Hines ML, Carnevale NT (1997) The NEURON simulation environment. Neural Comput 9(6):1179-1209.
49. Malenka RC, Bear MF (2004) LTP and LTD: An embarrassment of riches. Neuron 44(1):5-21.
50. Burkhalter A, Gonchar Y, Mellor RL, Nerbonne JM (2006) Differential expression of I(A) channel subunits Kv4.2 and Kv4.3 in mouse visual cortical neurons and synapses. J Neurosci 26(47):12274-12282.
51. Lai HC, Jan LY (2006) The distribution and targeting of neuronal voltage-gated ion channels. Nat Rev Neurosci 7(7):548-562.
52. Paspalas CD, Wang M, Arnsten AF (2013) Constellation of HCN channels and cAMP regulating proteins in dendritic spines of the primate prefrontal cortex: Potential substrate for working memory deficits in schizophrenia. Cereb Cortex 23(7):1643-1654.
53. Rall W (1974) Dendritic spines and synaptic potency. Studies in Neurophysiology, ed Porter R (Cambridge Univ Press, Cambridge, UK), pp 203-209.
54. Harvey CD, Svoboda K (2007) Locally dynamic synaptic learning rules in pyramidal neuron dendrites. Nature 450(7173):1195-1200.
55. Lee SJ, Escobedo-Lozoya Y, Szatmari EM, Yasuda R (2009) Activation of CaMKII in single dendritic spines during long-term potentiation. Nature 458(7236):299-304.
56. Tønnesen J, Katona G, Rózsa B, Nägerl UV (2014) Spine neck plasticity regulates compartmentalization of synapses. Nat Neurosci 17(5):678-685.
57. Charrier C, et al. (2012) Inhibition of SRGAP2 function by its human-specific paralogs induces neoteny during spine maturation. Cell 149(4):923-935.
58. Ryu J, et al. (2006) A critical role for myosin IIb in dendritic spine morphology and synaptic function. Neuron 49(2):175-182.
59. Holthoff K, Zecevic D, Konnerth A (2010) Rapid time course of action potentials in spines and remote dendrites of mouse visual cortex neurons. J Physiol 588(Pt): 1085-1096.
60. Palmer LM, Stuart GJ (2009) Membrane potential changes in dendritic spines during action potentials and synaptic input. J Neurosci 29(21):6897-6903.
61. Benavides-Piccione R, Ballesteros-Yáñez I, DeFelipe J, Yuste R (2002) Cortical area and species differences in dendritic spine morphology. J Neurocytol 31(3-5):337-346.
62. Johnston D,Wu S (1995) Foundations of Cellular Neurophysiology (MIT Press, Cambridge, MA).
63. Benke TA, Lüthi A, Isaac JT, Collingridge GL (1998) Modulation of AMPA receptor unitary conductance by synaptic activity. Nature 393(6687):793-797.