Synaptic clustering within dendrites: An emerging theory of memory formation

Progress in Neurobiology

Volumn 126, Issue , 2015, Pages 19-35

  Kastellakis, George ^a   Cai, Denise J ^b   Mednick, Sara C ^c   Silva, Alcino J ^b   Poirazi, Panayiota ^a  

^a INSTITUTE OF MOLECULAR BIOLOGY AND BIOTECHNOLOGY   (Greece)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Active dendrites; Associative memory; Plasticity; Synapse clustering; Synaptic tagging and capture

Indexed keywords

AMPA RECEPTOR; CALCIUM; MESSENGER RNA; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ARTIFICIAL NEURAL NETWORK; BRAIN CORTEX; BRAIN ELECTROPHYSIOLOGY; CELL MEMBRANE DEPOLARIZATION; COOPERATION; DENDRITE; EXCITATORY POSTSYNAPTIC POTENTIAL; GENETIC TRANSCRIPTION; HIPPOCAMPAL CA1 REGION; HIPPOCAMPUS; HOMEOSTASIS; HUMAN; LONG TERM POTENTIATION; MEMBRANE CONDUCTANCE; MEMORY CONSOLIDATION; MONOSYNAPTIC PATHWAY; NERVE CELL EXCITABILITY; NERVE CELL MEMBRANE; NERVE CELL PLASTICITY; NONHUMAN; PRIMARY AUDITORY CORTEX; PRIORITY JOURNAL; PROTEIN SYNTHESIS; PROTEIN SYNTHESIS INHIBITION; PYRAMIDAL NERVE CELL; REVIEW; SPIKE; SYNAPSE; ANIMAL; BRAIN; MEMORY; PATHOLOGY; PHYSIOLOGY;

ANIMALS; BRAIN; DENDRITES; HOMEOSTASIS; HUMANS; MEMORY; NEURONAL PLASTICITY; SYNAPSES;

EID: 84925500309     PISSN: 03010082     EISSN: 18735118     Source Type: Journal    
DOI: 10.1016/j.pneurobio.2014.12.002     Document Type: Review

References (165)

1. Abraham W.C. Metaplasticity: tuning synapses and networks for plasticity. Nat. Rev. Neurosci. 2008, 9(5):387. 10.1038/nrn2356.
2. Antic S.D., Zhou W.-L., Moore A.R., Short S.M., Ikonomu K.D. The decade of the dendritic NMDA spike. J. Neurosci. Res. 2010, 88(14):2991-3001. 10.1002/jnr.22444.
3. Archie K.A., Mel B.W. A model for intradendritic computation of binocular disparity. Nat. Neurosci. 2000, 3(1):54-63.
4. Ariav G., Polsky A., Schiller J. Submillisecond precision of the input-output transformation function mediated by fast sodium dendritic spikes in basal dendrites of CA1 pyramidal neurons. J. Neurosci. 2003, 23(21):7750-7758. Retrieved from: http://www.jneurosci.org/content/23/21/7750.short.
5. Ballarini F., Moncada D., Martinez M.C., Alen N., Viola H. Behavioral tagging is a general mechanism of long-term memory formation. Proc. Natl. Acad. Sci. U. S. A. 2009, 106(34):14599-14604. 10.1073/pnas.0907078106.
6. Bar-Ilan L., Gidon A., Segev I. The role of dendritic inhibition in shaping the plasticity of excitatory synapses. Front. Neural Circuits 2012, 6(April):118. 10.3389/fncir.2012.00118.
7. Baudry M., Bi X., Gall C., Lynch G. The biochemistry of memory: the 26 year journey of a new and specific hypothesis. Neurobiol. Learn. Mem. 2011, 95(2):125-133. 10.1016/j.nlm.2010.11.015.
8. Behabadi B.F., Mel B.W. Mechanisms underlying subunit independence in pyramidal neuron dendrites. Proc. Natl. Acad. Sci. U. S. A. 2014, 111(1):498-503.
9. Behabadi B.F., Polsky A., Jadi M., Schiller J., Mel B.W. Location-dependent excitatory synaptic interactions in pyramidal neuron dendrites. PLoS Comput. Biol. 2012, 8(7):e1002599. 10.1371/journal.pcbi.1002599.
10. Béïque J.-C., Na Y., Kuhl D., Worley P.F., Huganir R.L. Arc-dependent synapse-specific homeostatic plasticity. Proc. Natl. Acad. Sci. U. S. A. 2011, 108(2):816-821.
11. Bhalla U.S. Multiscale interactions between chemical and electric signaling in LTP induction, LTP reversal and dendritic excitability. Neural Netw. 2011, 24(9):943-949. 10.1016/j.neunet.2011.05.001.
12. Bleuler E., Zinkin J. Dementia Praecox or the Group of Schizophrenias 1950, International University Press, New York.
13. Bliss T.V.P., Collingridge G.L. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 1993, 361(6407):31-39.
14. Bodian D. A suggestive relationship of nerve cell RNA with specific synaptic sites. Proc. Natl. Acad. Sci. U. S. A. 1965, 53(2):418.
15. Boucher J., Cowell P., Howard M., Broks P., Farrant A., Roberts N., Mayes A. A combined clinical, neuropsychological, and neuroanatomical study of adults with high functioning autism. Cogn. Neuropsychiatry 2005, 10(3):165-213. pii:P01U93L300864771. 10.1080/13546800444000038.
16. Bourne J.N., Harris K.M. Nanoscale analysis of structural synaptic plasticity. Curr. Opin. Neurobiol. 2011, 22(3):1-11. 10.1016/j.conb.2011.10.019.
17. Bowler D.M., Gaigg S.B., Gardiner J.M. Multiple list learning in adults with autism spectrum disorder: parallels with frontal lobe damage or further evidence of diminished relational processing?. J. Autism Dev. Disord. 2010, 40(2):179-187.
18. Bowler D.M., Gardiner J.M., Grice S.J. Episodic memory and remembering in adults with Asperger syndrome. J. Autism Dev. Disord. 2000, 30(4):295-304. Retrieved from: http://www.ncbi.nlm.nih.gov/pubmed/11039856.
19. Bowler D.M., Matthews N.J., Gardiner J.M. Asperger's syndrome and memory: similarity to autism but not amnesia. Neuropsychologia 1997, 35(1):65-70. 10.1016/S0028-3932(96)00054-1.
20. Braitenberg V., Schüz A. Cortical architectonics. Cortex: Statistics and Geometry of Neuronal Connectivity 1998, 135-137. Springer, Berlin.
21. Branco T., Häusser M. The single dendritic branch as a fundamental functional unit in the nervous system. Curr. Opin. Neurobiol. 2010, 20(4):494-502. 10.1016/j.conb.2010.07.009.
22. Branco T., Häusser M. Synaptic integration gradients in single cortical pyramidal cell dendrites. Neuron 2011, 69(5):885-892. 10.1016/j.neuron.2011.02.006.
23. Cajigas J., Tushev G., Will T.J.J., Dieck S., Fuerst N., Schuman E.M.M., Tom Dieck S. The local transcriptome in the synaptic neuropil revealed by deep sequencing and high-resolution imaging. Neuron 2012, 74(3):453-466. 10.1016/j.neuron.2012.02.036.
24. Cash S., Yuste R. Linear summation of excitatory inputs by CA1 pyramidal neurons. Neuron 1999, 22(2):383-394. Retrieved from: http://www.ncbi.nlm.nih.gov/pubmed/10069343.
25. Chen J.L., Villa K.L., Cha J.W., So P.T.C., Kubota Y., Nedivi E. Clustered dynamics of inhibitory synapses and dendritic spines in the adult neocortex. Neuron 2012, 74(2):361-373. 10.1016/j.neuron.2012.02.030.
26. Chen X., Leischner U., Rochefort N.L.N.L., Nelken I., Konnerth A. Functional mapping of single spines in cortical neurons in vivo. Nature 2011, 475(7357):501-505. 10.1038/nature10193.
27. Chiu C.Q., Lur G., Morse T.M., Carnevale N.T., Ellis-Davies G.C.R., Higley M.J. Compartmentalization of GABAergic inhibition by dendritic spines. Science 2013, 340(6133):759-762.
28. Chklovskii D.B.B., Mel B.W., Svoboda K. Cortical rewiring and information storage. Nature 2004, 431(7010):782-788. Retrieved from: http://www.nature.com/nature/journal/v431/n7010/abs/nature03012.html.
29. Citri A., Malenka R.C. Synaptic plasticity: multiple forms, functions, and mechanisms. Neuropsychopharmacology 2008, 33(1):18-41. 10.1038/sj.npp.1301559.
30. Clopath C., Ziegler L., Vasilaki E., Büsing L., Gerstner W. Tag-trigger-consolidation: a model of early and late long-term-potentiation and depression. PLoS Comput. Biol. 2008, 4(12):e1000248. 10.1371/journal.pcbi.1000248.
31. Cutsuridis V., Cobb S., Graham B.P. Encoding and retrieval in a model of the hippocampal CA1 microcircuit. Hippocampus 2010, 20(3):423-446.
32. Das T., Ivleva E.I., Wagner A.D., Stark C.E.L., Tamminga C.A. Loss of pattern separation performance in schizophrenia suggests dentate gyrus dysfunction. Schizophr. Res. 2014, 159(1):193-197. 10.1016/j.schres.2014.05.006.
33. De Carvalho Myskiw J., Benetti F., Izquierdo I. Behavioral tagging of extinction learning. Proc. Natl. Acad. Sci. U. S. A. 2013, 110(3):1071-1076. 10.1073/pnas.1220875110.
34. DeBello W.M., McBride T.J., Nichols G.S., Pannoni K.E., Sanculi D., Totten D.J. Input clustering and the microscale structure of local circuits. Front. Neural Circuits 2014, 8:112. 10.3389/fncir.2014.00112.
35. Druckmann S., Feng L., Lee B., Yook C., Zhao T., Magee J.C., Kim J. Structured synaptic connectivity between hippocampal regions. Neuron 2014, 81(3):629-640.
36. 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(8):e700. 10.1371/journal.pone.0000700.
37. Frey U., Morris R.G.M.G. Synaptic tagging and long-term potentiation. Nature 1997, 385(6616):533-536. 10.1038/385533a0.
38. Frick A., Magee J., Johnston D. LTP is accompanied by an enhanced local excitability of pyramidal neuron dendrites. Nat. Neurosci. 2004, 7(2):126-135. 10.1038/nn1178.
39. Fu M., Yu X., Lu J., Zuo Y. Repetitive motor learning induces coordinated formation of clustered dendritic spines in vivo. Nature 2012, 1(7387):92-95. 10.1038/nature10844.
40. Garner A.R., Rowland D.C., Hwang S.Y., Baumgaertel K., Roth B.L., Kentros C., Mayford M. Generation of a synthetic memory trace. Science (New York, N.Y.) 2012, 335(6075):1513-1516. 10.1126/science.1214985.
41. Gasparini S., Migliore M., Magee J.C. On the initiation and propagation of dendritic spikes in CA1 pyramidal neurons. J. Neurosci. 2004, 24(49):11046-11056. 10.1523/JNEUROSCI.2520-04.2004.
42. Gold P.E. Protein synthesis inhibition and memory: formation vs amnesia. Neurobiol. Learn. Mem. 2008, 89(3):201-211.
43. Golding N.L., Staff N.P., Spruston N. Dendritic spikes as a mechanism for cooperative long-term potentiation. Nature 2002, 418(6895):326-331.
44. Gómez González J.F., Mel B.W., Poirazi P. Distinguishing linear vs. non-linear integration in CA1 radial oblique dendrites: it's about time. Front. Comput. Neurosci. 2011, 5:44. 10.3389/fncom.2011.00044.
45. Govindarajan A., Israely I., Huang S.-Y., Tonegawa S. The dendritic branch is the preferred integrative unit for protein synthesis-dependent LTP. Neuron 2011, 69(1):132-146. 10.1016/j.neuron.2010.12.008.
46. Govindarajan A., Kelleher R.J., Tonegawa S. A clustered plasticity model of long-term memory engrams. Nat. Rev. Neurosci. 2006, 7(7):575-583. 10.1038/nrn1937.
47. Han J.-H., Kushner S.A., Yiu A.P., Cole C.J., Matynia A., Brown R.A., Josselyn S.A. Neuronal competition and selection during memory formation. Science (New York, N.Y.) 2007, 316(5823):457-460. 10.1126/science.1139438.
48. Hardie J., Spruston N. Synaptic depolarization is more effective than back-propagating action potentials during induction of associative long-term potentiation in hippocampal pyramidal neurons. J. Neurosci. 2009, 29(10):3233-3241. 10.1523/JNEUROSCI.6000-08.2009.
49. Harvey C.D., Svoboda K. Locally dynamic synaptic learning rules in pyramidal neuron dendrites. Nature 2007, 450(7173):1195-1200. 10.1038/nature06416.
50. Harvey C.D., Yasuda R., Zhong H., Svoboda K. The spread of Ras activity triggered by activation of a single dendritic spine. Science (New York, N.Y.) 2008, 321(5885):136-140. 10.1126/science.1159675.
51. Häusser M., Mel B., Hausser M. Dendrites: bug or feature?. Curr. Opin. Neurobiol. 2003, 13(3):372-383. 10.1016/S0959-4388(03)00075-8.
52. Häusser M., Spruston N., Stuart G.J. Diversity and dynamics of dendritic signaling. Science 2000, 290(5492):739-744.
53. Hebb D.O. The Organization of Behavior 1949, Wiley, New York.
54. Hering H., Sheng M. Dendritic spines: structure, dynamics and regulation. Nat. Rev. Neurosci. 2001, 2(12):880-888. 10.1038/35104061.
55. Hopfield J.J. Artificial neural networks. Circuits Devices Mag. IEEE 1988, 4(5):3-10.
56. Hou Q., Gilbert J., Man H.-Y. Homeostatic regulation of AMPA receptor trafficking and degradation by light-controlled single-synaptic activation. Neuron 2011, 72(5):806-818. 10.1016/j.neuron.2011.10.011.
57. Huang Y.-Y., Kandel E.R. 5-Hydroxytryptamine induces a protein kinase A/mitogen-activated protein kinase-mediated and macromolecular synthesis-dependent late phase of long-term potentiation in the amygdala. J. Neurosci. 2007, 27(12):3111-3119.
58. Huang Z.J., Kirkwood A., Pizzorusso T., Porciatti V., Morales B., Bear M.F., Tonegawa S. BDNF regulates the maturation of inhibition and the critical period of plasticity in mouse visual cortex. Cell 1999, 98(6):739-755.
59. Hübener M., Bonhoeffer T. Searching for engrams. Neuron 2010, 67(3):363-371. 10.1016/j.neuron.2010.06.033.
60. Iannella N., Tanaka S. Synaptic efficacy cluster formation across the dendrite via STDP. Neurosci. Lett. 2006, 403(1):24-29.
61. Izquierdo I., Bevilaqua L.R.M., Rossato J.I., Bonini J.S., Medina J.H., Cammarota M. Different molecular cascades in different sites of the brain control memory consolidation. Trends Neurosci. 2006, 29(9):496-505.
62. Jadi M.P., Behabadi B.F., Poleg-Polsky A., Schiller J., Mel B.W. An augmented two-layer model captures nonlinear analog spatial integration effects in pyramidal neuron dendrites. Proc. IEEE 2014, 102(5):782-798. (Special issue on Computational Neuroscience).
63. Jadi M., Polsky A., Schiller J., Mel B.W. Location-dependent effects of inhibition on local spiking in pyramidal neuron dendrites. PLoS Comput. Biol. 2012, 8(6):e1002550.
64. Jia H., Rochefort N.L., Chen X., Konnerth A. Dendritic organization of sensory input to cortical neurons in vivo. Nature 2010, 464(7293):1307-1312. 10.1038/nature08947.
65. Josselyn S. Continuing the search for the engram: examining the mechanism of fear memories. J. Psychiatry Neurosci. 2010, 35(4):221-228. 10.1503/jpn.100015.
66. Kang H., Schuman E.M. A requirement for local protein synthesis in neurotrophin-induced hippocampal synaptic plasticity. Science 1996, 273(5280):1402-1406.
67. Katz Y., Menon V., Nicholson D.A., Geinisman Y., Kath W.L., Spruston N. Synapse distribution suggests a two-stage model of dendritic integration in CA1 pyramidal neurons. Neuron 2009, 63(2):171-177. 10.1016/j.neuron.2009.06.023.
68. Kelleher R.J., Govindarajan A., Tonegawa S. Translational regulatory mechanisms in persistent forms of synaptic plasticity. Neuron 2004, 44(1):59-73. 10.1016/j.neuron.2004.09.013.
69. Kim J., Kwon J.-T., Kim H.-S., Josselyn S.A., Han J.-H. Memory recall and modifications by activating neurons with elevated CREB. Nat. Neurosci. 2014, 17(1):65-72.
70. Kim S., Guzman S.J., Hu H., Jonas P. Active dendrites support efficient initiation of dendritic spikes in hippocampal CA3 pyramidal neurons. Nat. Neurosci. 2012, 15(4):600-606. 10.1038/nn.3060.
71. Klausberger T., Somogyi P. Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations. Science 2008, 321(5885):53-57.
72. Kleindienst T., Winnubst J., Roth-Alpermann C., Bonhoeffer T., Lohmann C. Activity-dependent clustering of functional synaptic inputs on developing hippocampal dendrites. Neuron 2011, 72(6):1012-1024. 10.1016/j.neuron.2011.10.015.
73. Kramár E.A., Babayan A.H., Gavin C.F., Cox C.D., Jafari M., Gall C.M., Lynch G. Synaptic evidence for the efficacy of spaced learning. Proc. Natl. Acad. Sci. U. S. A. 2012, 109(13):5121-5126. 10.1073/pnas.1120700109.
74. Kullmann D.M., Moreau A.W., Bakiri Y., Nicholson E. Plasticity of inhibition. Neuron 2012, 75(6):951-962. 10.1016/j.neuron.2012.07.030.
75. Labno A., Warrier A., Wang S., Zhang X. Local plasticity of dendritic excitability can be autonomous of synaptic plasticity and regulated by activity-based phosphorylation of Kv4.2. PLoS ONE 2014, 9(1):e84086.
76. Larkum M.E., Nevian T. Synaptic clustering by dendritic signalling mechanisms. Curr. Opin. Neurobiol. 2008, 18(3):321-331. 10.1016/j.conb.2008.08.013.
77. Larkum M.E., Nevian T., Sandler M., Polsky A., Schiller J., Larkum Nevian T., Sandler M., Polsky A., Schiller J.M.E. Synaptic integration in tuft dendrites of layer 5 pyramidal neurons: a new unifying principle. Science 2009, 325(5941):756-760.
78. Larkum M.E., Zhu J.J. Signaling of layer 1 and whisker-evoked Ca2+ and Na+ action potentials in distal and terminal dendrites of rat neocortical pyramidal neurons in vitro and in vivo. J. Neurosci. 2002, 22(16):6991-7005.
79. Lashley K.S. In search of the engram. Symposia of the Society for Experimental 1950, Retrieved from: http://homepage.mac.com/sanagnos/lashley1950.pdf.
80. Lavzin M., Rapoport S., Polsky A., Garion L., Schiller J. Nonlinear dendritic processing determines angular tuning of barrel cortex neurons in vivo. Nature 2012, 490(7420):397-401. 10.1038/nature11451.
81. Lee Y.-S., Silva A.J. The molecular and cellular biology of enhanced cognition. Nat. Rev. Neurosci. 2009, 10(2):126-140. 10.1038/nrn2572.
82. Legenstein R., Maass W. Branch-specific plasticity enables self-organization of nonlinear computation in single neurons. J. Neurosci. 2011, 31(30):10787-10802. 10.1523/JNEUROSCI.5684-10.2011.
83. Liao D., Hessler N.A., Malinow R. Activation of postsynaptically silent synapses during pairing-induced LTP in CA1 region of hippocampal slice. Nature 1995, 375(6530):400-403.
84. Liu G. Local structural balance and functional interaction of excitatory and inhibitory synapses in hippocampal dendrites. Nat. Neurosci. 2004, 7(4):373-379. 10.1038/nn1206 nn1206.
85. Liu X., Ramirez S., Pang P.T., Puryear C.B., Govindarajan A., Deisseroth K., Tonegawa S. Optogenetic stimulation of a hippocampal engram activates fear memory recall. Nature 2012, 484(7394):381-385. 10.1038/nature11028.
86. Longordo F., To M., Ikeda K., Stuart G. Sublinear integration underlies binocular processing in primary visual cortex. Nat. Neurosci. 2013, 16(6):714-723. 10.1038/nn.3394.
87. Losonczy A., Magee J.C. Integrative properties of radial oblique dendrites in hippocampal CA1 pyramidal neurons. Neuron 2006, 50(2):291-307. 10.1016/j.neuron.2006.03.016.
88. Losonczy A., Makara J.K., Magee J.C. Compartmentalized dendritic plasticity and input feature storage in neurons. Nature 2008, 452(7186):436-441. 10.1038/nature06725.
89. Lovett-Barron M., Turi G.F., Kaifosh P., Lee P.H., Bolze F., Sun X.-H., Losonczy A. Regulation of neuronal input transformations by tunable dendritic inhibition. Nat. Neurosci. 2012, 15(3):423-430. 10.1038/nn.3024S1-3.
90. Ludwig M. Dendritic Neurotransmitter Release 2005, Springer, Berlin.
91. Mainen Z., Sejnowski T. Influence of dendritic structure on firing pattern in model neocortical neurons. Nature 1996, Retrieved from: http://papers.cnl.salk.edu/PDFs/Influence of Dendritic Structure on Firing Pattern in Model Neocortical Neurons 1996-3205.pdf.
92. Major G., Larkum M.E., Schiller J. Active properties of neocortical pyramidal neuron dendrites. Ann. Rev. Neurosci. 2013, 36:1-24. 10.1146/annurev-neuro-062111-150343.
93. Makara J.K., Losonczy A., Wen Q., Magee J.C. Experience-dependent compartmentalized dendritic plasticity in rat hippocampal CA1 pyramidal neurons. Nat. Neurosci. 2009, 12(12):1485-1487. 10.1038/nn.2428.
94. Makara J.K., Magee J.C. Variable dendritic integration in hippocampal CA3 pyramidal neurons. Neuron 2013, 80(6):1438-1450.
95. Makino H., Malinow R. Article compartmentalized versus global synaptic plasticity on dendrites controlled by experience. Neuron 2011, 72(6):1001-1011. 10.1016/j.neuron.2011.09.036.
96. Manschreck T.C., Maher B.A., Milavetz J.J., Ames D., Weisstein C.C., Schneyer M.L. Semantic priming in thought disordered schizophrenic patients. Schizophr. Res. 1988, 1(1):61-66. 10.1016/0920-9964(88)90041-2.
97. McBride T.J., Rodriguez-Contreras A., Trinh A., Bailey R., DeBello W.M. Learning drives differential clustering of axodendritic contacts in the barn owl auditory system. J. Neurosci. 2008, 28(27):6960-6973.
98. McClelland J.L., Rumelhart D.E. A distributed model of human learning and memory. Parallel Distributed Processing: Explorations in the Microstructure of Cognition 1986, vol. 2:170-215. MIT Press, Cambridge.
99. Megias M., Emri Z.S., Freund T.F., Gulyas A.I. Total number and distribution of inhibitory and excitatory synapses on hippocampal CA1 pyramidal cells. Neuroscience 2001, 102(3):527-540.
100. Mel B.W. The clusteron: toward a simple abstraction for a complex neuron. Advances in Neural Information Processing Systems 1991, 35-42. Morgan Kaufmann, San Mateo.
101. Mel B.W. NMDA-based pattern discrimination in a modeled cortical neuron. Neural Comput. 1992, 4(4):502-517. 10.1162/neco.1992.4.4.502.
102. Mel B.W. Synaptic integration in an excitable dendritic tree. J. Neurophysiol. 1993, 70(3):1086-1101. Retrieved from: http://www.ncbi.nlm.nih.gov/pubmed/8229160.
103. Mel B.W., Ruderman D.L., Archie K.A. Translation-invariant orientation tuning in visual complex cells could derive from intradendritic computations. J. Neurosci. 1998, 18(11):4325-4334. Retrieved from: http://www.jneurosci.org/cgi/content/abstract/18/11/4325.
104. Migliore M., Novara G., Tegolo D. Single neuron binding properties and the magical number 7. Hippocampus 2008, 18(11):1122-1130.
105. Minsky M., Papert S. Perceptron: An Introduction to Computational Geometry 1969, vol. 19:88. The MIT Press, Cambridge. Expanded edition.
106. Moncada D., Viola H. Induction of long-term memory by exposure to novelty requires protein synthesis: evidence for a behavioral tagging. J. Neurosci. 2007, 27(28):7476-7481. 10.1523/JNEUROSCI.1083-07.2007.
107. Morita K. Possible role of dendritic compartmentalization in the spatial working memory circuit. J. Neurosci. 2008, 28(30):7699-7724. 10.1523/JNEUROSCI.0059-08.2008.
108. Murakoshi H., Wang H., Yasuda R. Local, persistent activation of Rho GTPases during plasticity of single dendritic spines. Nature 2011, 472(7341):100-104.
109. Murakoshi H., Yasuda R. Postsynaptic signaling during plasticity of dendritic spines. Trends Neurosci. 2012, 35(2):135-143. 10.1016/j.tins.2011.12.002.
110. Nevian T., Larkum M.E., Polsky A., Schiller J. Properties of basal dendrites of layer 5 pyramidal neurons: a direct patch-clamp recording study. Nat. Neurosci. 2007, 10(2):206-214. 10.1038/nn1826.
111. O'Connor N., Hermelin B. Low intelligence and special abilities. J. Child Psychol. Psychiatry 1988, 29(4):391-396. Retrieved from: http://www.ncbi.nlm.nih.gov/pubmed/3063716.
112. O'Donnell C., Sejnowski T.J., O'Donnell C. Selective memory generalization by spatial patterning of protein synthesis. Neuron 2014, 82(2):398-412. 10.1016/j.neuron.2014.02.028.
113. Papoutsi A., Sidiropoulou K., Poirazi P. Dendritic nonlinearities reduce network size requirements and mediate on and off states of persistent activity in a pfc microcircuit model. PLoS Comput. Biol. 2014, 10(7):e1003764. 10.1371/journal.pcbi.1003764.
114. Papoutsi A., Sidiropoulou K., Cutsuridis V., Poirazi P. Induction and modulation of persistent activity in a layer V PFC microcircuit model. Front. Neural Circuits 2013, 7(October):161. 10.3389/fncir.2013.00161.
115. Papoutsi A., Sidiropoulou K., Poirazi P. Memory Beyond Synaptic Plasticity: The Role of Intrinsic Neuronal Excitability. Memory Mechanisms in Health and Disease: Mechanistic Basis of Memory 2012, 444. World Scientific Pub. Co. Inc., Retrieved from: http://www.amazon.com/Memory-Mechanisms-Health-Disease-Mechanistic/dp/9814366692. 1st ed.
116. Patterson M., Yasuda R. Signalling pathways underlying structural plasticity of dendritic spines. Spine 2011, 1. 10.1111/j.1476-5381.2011.01328.x.
117. Peters A., Paley S.L., de Webster H.F. The Fine Structure of the Nervous System 1976, Saunders, Philadelphia.
118. Poirazi P., Brannon T., Mel B.W. Arithmetic of subthreshold synaptic summation in a model CA1 pyramidal cell. Neuron 2003, 37(6):977-987. Retrieved from: http://www.ncbi.nlm.nih.gov/pubmed/12670426.
119. Poirazi P., Brannon T., Mel B.W. Pyramidal neuron as two-layer neural network. Neuron 2003, 37(6):989-999. Retrieved from: http://www.ncbi.nlm.nih.gov/pubmed/12670427.
120. Poirazi P., Mel B.W. Impact of active dendrites and structural plasticity on the memory capacity of neural tissue. Neuron 2001, 29:779-796.
121. Poljakov J. Schizophrenie und Erkenntnistatigkeit 1973, Hippokrates, Stuttgart, Germany.
122. Polsky A., Mel B.W., Schiller J. Computational subunits in thin dendrites of pyramidal cells. Nat. Neurosci. 2004, 7(6):621-627. 10.1038/nn1253.
123. Pozo K., Goda Y. Unraveling mechanisms of homeostatic synaptic plasticity. Neuron 2010, 66(3):337-351. 10.1016/j.neuron.2010.04.028.
124. Rabinowitch I., Segev I. Two opposing plasticity mechanisms pulling a single synapse. Trends Neurosci. 2008, 31(8):377-383. 10.1016/j.tins.2008.05.005.
125. Ramón y Cajal S. Neue Darstellung vom histologischen Bau den Centralnervensystems. Arch. Anat. Entwick 1893, 5(6):319-428.
126. Redondo R.L., Morris R.G.M. Making memories last: the synaptic tagging and capture hypothesis. Nat. Rev. Neurosci. 2011, 12(1):17-30. 10.1038/nrn2963.
127. Reymann K.G., Frey J.U. The late maintenance of hippocampal LTP: requirements, phases, synaptic tagging, late-associativity and implications. Neuropharmacology 2007, 52(1):24-40. 10.1016/j.neuropharm.2006.07.026.
128. Rogerson T., Cai D.J., Frank A., Sano Y., Shobe J., Lopez-Aranda M.F., Silva A.J. Synaptic tagging during memory allocation. Nat. Rev. Neurosci. 2014, 15:157-169. 10.1038/nrn3667.
129. Routtenberg A., Rekart J.L. Post-translational protein modification as the substrate for long-lasting memory. Trends Neurosci. 2005, 28(1):12-19.
130. Sajikumar S., Frey J.U. Late-associativity, synaptic tagging, and the role of dopamine during LTP and LTD. Neurobiol. Learn. Mem. 2004, 82(1):12-25. 10.1016/j.nlm.2004.03.003.
131. Salmond C.H., Ashburner J., Connelly A., Friston K.J., Gadian D.G., Vargha-Khadem F. The role of the medial temporal lobe in autistic spectrum disorders. Eur. J. Neurosci. 2005, 22(3):764-772. pii:EJN4217. 10.1111/j.1460-9568.2005.04217.x.
132. Schiller J., Major G., Koester H.J., Schiller Y. NMDA spikes in basal dendrites. Nature 2000, 1261(1997):285-289.
133. Schiller J., Major G., Koester H.J., Schiller Y. NMDA spikes in basal dendrites of cortical pyramidal neurons. Nature 2000, 404(6775):285-289. 10.1038/35005094.
134. Schiller J., Schiller Y., Stuart G., Sakmann B. Calcium action potentials restricted to distal apical dendrites of rat neocortical pyramidal neurons. J. Physiol. 1997, 505(3):605-616.
135. Schuemann A., Klawiter A., Bonhoeffer T., Wierenga C.J. Structural plasticity of GABAergic axons is regulated by network activity and GABAA receptor activation. Front. Neural Circuits 2013, 7(June):113. 10.3389/fncir.2013.00113.
136. Segev I. Untangling dendrites with quantitative models. Science 2000, 290(5492):744-750. 10.1126/science.290.5492.744.
137. Segev I., Rall W. Excitable dendrites and spines: earlier theoretical insights elucidate recent direct observations. Trends Neurosci. 1998, 21(11):453-460. 10.1016/S0166-2236(98)01327-7.
138. Sidiropoulou K., Poirazi P. Predictive features of persistent activity emergence in regular spiking and intrinsic bursting model neurons. PLoS Comput. Biol. 2012, 8(4):e1002489. 10.1371/journal.pcbi.1002489.
139. Silva A.J., Zhou Y., Rogerson T., Shobe J., Balaji J. Molecular and cellular approaches to memory allocation in neural circuits. Science (New York, N.Y.) 2009, 326(5951):391-395. 10.1126/science.1174519.
140. Silver R.A. Neuronal arithmetic. Nat. Rev. Neurosci. 2010, 11(7):474-489. 10.1038/nrn2864.
141. Sjöström P.J., Rancz E.A., Roth A., Häusser M. Dendritic excitability and synaptic plasticity. Physiol. Rev. 2008, 88(2):769-840. 10.1152/physrev.00016.2007.
142. Sjöström P.J., Turrigiano G.G., Nelson S.B. Rate, timing, and cooperativity jointly determine cortical synaptic plasticity. Neuron 2001, 32(6):1149-1164. Retrieved from: http://www.ncbi.nlm.nih.gov/pubmed/11754844.
143. Smith B.J., Gardiner J.M., Bowler D.M. Deficits in free recall persist in Asperger's syndrome despite training in the use of list-appropriate learning strategies. J. Autism Dev. Disord. 2007, 37(3):445-454. 10.1007/s10803-006-0180-4.
144. Smith S.L., Smith I.T., Branco T., Häusser M. Dendritic spikes enhance stimulus selectivity in cortical neurons in vivo. Nature 2013, 503(7474):115-120. 10.1038/nature12600.
145. Spruston N. Pyramidal neurons: dendritic structure and synaptic integration. Nat. Rev. Neurosci. 2008, 9(3):206-221. 10.1038/nrn2286.
146. Steward O., Levy W.B. Preferential localization of polyribosomes under the base of dendritic spines in granule cells of the dentate gyrus. J. Neurosci. 1982, 2(3):284-291.
147. Steward O., Schuman E.M. Protein synthesis at synaptic sites on dendrites. Handbook of Neurochemistry and Neurobiology 2007, 169-195. Springer, US.
148. Sutton M.A., Ito H.T., Cressy P., Kempf C., Woo J.C., Schuman E.M. Miniature neurotransmission stabilizes synaptic function via tonic suppression of local dendritic protein synthesis. Cell 2006, 125(4):785-799. 10.1016/j.cell.2006.03.040.
149. Sutton M.A., Schuman E.M. Dendritic protein synthesis, synaptic plasticity, and memory. Cell 2006, 127(1):49-58. 10.1016/j.cell.2006.09.014.
150. Takahashi N., Kitamura K., Matsuo N., Mayford M., Kano M., Matsuki N., Ikegaya Y. Locally synchronized synaptic inputs. Science (New York, N.Y.) 2012, 335(6066):353-356. 10.1126/science.1210362.
151. Trachtenberg J.T., Chen B.E., Knott G.W., Feng G., Sanes J.R., Welker E., Svoboda K. Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex. Nature 2002, 420(6917):788-794. 10.1038/nature01273.
152. Treffert D.A. The savant syndrome: an extraordinary condition. A synopsis: past, present, future. Philos. Trans. R. Soc. B: Biol. Sci. 2009, 364(1522):1351-1357.
153. Turrigiano G.G., Nelson S.B. Homeostatic plasticity in the developing nervous system. Nat. Rev. Neurosci. 2004, 5(2):97-107. 10.1038/nrn1327.
154. Varga Z., Jia H., Sakmann B., Konnerth A. Dendritic coding of multiple sensory inputs in single cortical neurons in vivo. Proc. Natl. Acad. Sci. U. S. A. 2011, 108(37). 10.1073/pnas.1112355108.
155. Vogels T.P., Abbott L.F. Gating multiple signals through detailed balance of excitation and inhibition in spiking networks. Nat. Neurosci. 2009, 12(4):483-491.
156. Wang Z., Xu N., Wu C., Duan S., Poo M. Bidirectional changes in spatial dendritic integration accompanying long-term synaptic modifications. Neuron 2003, 37(3):463-472. 10.1016/S0896-6273(02)01189-3.
157. Wei D.S., Mei Y.A., Bagal A., Kao J.P., Thompson S.M., Tang C.M. Compartmentalized and binary behavior of terminal dendrites in hippocampal pyramidal neurons. Science (New York, N.Y.) 2001, 293(5538):2272-2275. 10.1126/science.1061198.
158. Williams D.L., Goldstein G., Minshew N.J. The profile of memory function in children with autism. Neuropsychology 2006, 20(1):21-29. pii:2006-01440-003. 10.1037/0894-4105.20.1.21.
159. Winnubst J., Lohmann C., Jontes J., Wang H., Niell C. Synaptic clustering during development and learning: the why, when, and how. Front. Mol. Neurosci. 2012, 5(May):70. 10.3389/fnmol.2012.00070.
160. Wu G.-Y., Deisseroth K., Tsien R.W. Spaced stimuli stabilize MAPK pathway activation and its effects on dendritic morphology. Nat. Neurosci. 2001, 4(2):151-158.
161. Wu X.E., Mel B.W. Capacity-enhancing synaptic learning rules in a medial temporal lobe online learning model. Neuron 2009, 62(1):31-41. 10.1016/j.neuron.2009.02.021.
162. Yadav A., Gao Y.Z., Rodriguez A., Dickstein D.L., Susan L., Luebke J.I., Wearne S.L. Morphologic evidence for spatially clustered spines in apical dendrites of monkey neocortical pyramidal cells. J. Comp. Neurol. 2012, 520(13):2888-2902. 10.1002/cne.23070.
163. Yang G., Lai C.S.W., Cichon J., Ma L., Li W., Gan W.-B. Sleep promotes branch-specific formation of dendritic spines after learning. Science (New York, N.Y.) 2014, 344(6188):1173-1178. 10.1126/science.1249098.
164. Yuste R. Dendritic spines and distributed circuits. Neuron 2011, 71(5):772-781. 10.1016/j.neuron.2011.07.024.
165. Zhang W., Linden D.J. The other side of the engram: experience-driven changes in neuronal intrinsic excitability. Nat. Rev. Neurosci. 2003, 4(11):885-900. 10.1038/nrn1248.