Heterosynaptic plasticity: Multiple mechanisms and multiple roles

Neuroscientist

Volumn 20, Issue 5, 2014, Pages 483-498

  Chistiakova, Marina ^a   Bannon, Nicholas M ^a   Bazhenov, Maxim ^b   Volgushev, Maxim ^a  

^a UNIVERSITY OF CONNECTICUT   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

heterosynaptic plasticity; neocortex; neuron model; runaway dynamics; synaptic plasticity; weight normalization

Indexed keywords

LEARNING; LONG TERM POTENTIATION; NEOCORTEX; NERVE CELL EXCITABILITY; NERVE CELL PLASTICITY; POSTSYNAPTIC POTENTIAL; REVIEW; ANIMAL; PHYSIOLOGY; SYNAPSE;

ANIMALS; NEURONAL PLASTICITY; SYNAPSES;

EID: 84907210224     PISSN: 10738584     EISSN: 10894098     Source Type: Journal    
DOI: 10.1177/1073858414529829     Document Type: Review

References (109)

1. Abbott LF, Nelson SB. Synaptic plasticity: taming the beast. Nature Neurosci. 2000 ; 3: 1178-83
2. Abraham WC, Bear MF. Metaplasticity: the plasticity of synaptic plasticity. Trends Neurosci. 1996 ; 19 (4). 126-30
3. Arami MK, Sohya K, Sarihi A, Jiang B, Yanagawa Y. Reciprocal homosynaptic and heterosynaptic long-term plasticity of corticogeniculate projection neurons in layer VI of the mouse visual cortex. J Neurosci. 2013 ; 33 (18). 7787-98
4. Bauer EP, LeDoux JE. Heterosynaptic long-term potentiation of inhibitory interneurons in the lateral amygdala. J Neurosci. 2004 ; 24: 9507-12
5. Berridge MJ. Neuronal calcium signaling. Neuron. 1998 ; 21: 13-26
6. Bienenstock EL, Cooper LN, Munro PW. Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex. J Neurosci. 1982 ; 2: 32-48
7. Birtoli B, Ulrich D. Firing mode-dependent synaptic plasticity in rat neocortical pyramidal neurons. J Neurosci. 2004 ; 24: 4935-40
8. Bliss TV, Collingridge GL. A synaptic model of memory: long-term potentiation in the hippocampus. Nature. 1993 ; 361: 31-9
9. Bliss TV, Lomo T. Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol. 1973 ; 232: 331-56
10. Böhme GA, Bon C, Stutzmann JM, Doble A, Blanchard JC. Possible involvement of nitric oxide in long-term potentiation. Eur J Pharmacol. 1991 ; 199 (3). 379-81
11. Bonhoeffer T, Staiger V, Aersten A. Synaptic plasticity in rat hippocampal slice cultures: local "Hebbian" conjunction of pre- and postsynaptic stimulation leads to distributed synaptic enhancement. Proc Natl Acad Sci U S A. 1989 ; 86: 8113-7
12. Burrone J, O'Byrne M, Murthy VN. Multiple forms of synaptic plasticity triggered by selective suppression of activity in individual neurons. Nature. 2002 ; 420: 414-8
13. Caporale N, Dan Y. Spike timing-dependent plasticity: a Hebbian learning rule. Annu Rev Neurosci. 2008 ; 31: 25-46
14. Chen J, Tan Z, Zeng L, Zhang X, He Y, Gao W. Heterosynaptic long-term depression mediated by ATP released from astrocytes. Glia. 2013a ; 61 (2). 178-91
15. Chen JY, Lonjers P, Lee C, Chistiakova M, Volgushev M, Bazhenov M. Heterosynaptic plasticity prevents runaway synaptic dynamics. J Neurosci. 2013b ; 33 (40). 15915-29
16. Chevaleyre V, Castillo PE. Heterosynaptic LTD of hippocampal GABAergic synapses: a novel role of endocannabinoids in regulating excitability. Neuron. 2003 ; 38 (3). 461-72
17. Chevaleyre V, Takahashi KA, Castillo PE. Endocannabinoid-mediated synaptic plasticity in the CNS. Annu Rev Neurosci. 2006 ; 29: 37-76
18. Chistiakova M, Volgushev M. Heterosynaptic plasticity in the neocortex. Exp Brain Res. 2009 ; 199 (3-4). 377-90
19. Chiu CQ, Puente N, Grandes P, Castillo PE. Dopaminergic modulation of endocannabinoid-mediated plasticity at GABAergic synapses in the prefrontal cortex. J Neurosci. 2010 ; 30 (21). 7236-48
20. Christofi G, Nowicky AV, Bolsover SR, Bindman LJ. The postsynaptic induction of nonassociative long-term depression of excitatory synaptic transmission in rat hippocampal slices. J Neurophysiol. 1993 ; 69: 219-29
21. Cummings JA, Mulkey RM, Nicoll RA, Malenka RC. Ca2+ signaling requirements for long-term depression in the hippocampus. Neuron. 1996 ; 16 (4). 825-33
22. Daw MI, Bortolotto ZA, Saulle E, Zaman S, Collingridge GL, Isaac JT. Phosphatidylinositol 3 kinase regulates synapse specificity of hippocampal long-term depression. Nat Neurosci. 2002 ; 5: 835-6
23. Dudman JT, Tsay D, Siegelbaum SA. A role for synaptic inputs at distal dendrites: instructive signals for hippocampal long-term plasticity. Neuron. 2007 ; 56: 866-79
24. Elliott T, Shadbolt NR. Multiplicative synaptic normalization and a nonlinear Hebb rule underlie a neurotrophic model of competitive synaptic plasticity. Neural Comput. 2002 ; 14: 1311-22
25. Engert F, Bonhoeffer T. Synapse specificity of long-term potentiation breaks down at short distances. Nature. 1997 ; 388: 279-84
26. Fagni L, Chavis P, Ango F, Bockaert J. Complex interactions between mGluRs, intracellular Ca2+ stores and ion channels in neurons. Trends Neurosci. 2000 ; 23 (2). 80-8
27. Feldman DE. Timing-based LTP and LTD at vertical imputs to layer II/III pyramidal cells in rat barrel cortex. Neuron. 2000 ; 27: 45-56
28. Feldman DE. Synaptic mechanisms for plasticity in neocortex. Annu Rev Neurosci. 2009 ; 32: 33-55
29. Finelli LA, Haney S, Bazhenov M, Stopfer M, Sejnowski TJ. Synaptic learning rules and sparse coding in a model sensory system. PLoS Comput Biol. 2008 ; 4 (4). e1000062
30. Fink AE, O'Dell TJ. Short trains of theta frequency stimulation enhance CA1 pyramidal neuron excitability in the absence of synaptic potentiation. J Neurosci. 2009 ; 29 (36). 11203-14
31. Fonseca R, Nägerl UV, Morris GM, Bonhoeffer T. Competing for memory: hippocampal LTP under regimes of reduced protein synthesis. Neuron. 2004 ; 44: 1011-20
32. Frey U, Morris RGM. Synaptic tagging and long-term potentiation. Nature. 1997 ; 385 (6). 533-6
33. Frick A, Magee J, Johnston D. LTP is accompanied by an enhanced local excitability of pyramidal neuron dendrites. Nat Neurosci. 2004 ; 7: 126-35
34. Froemke RC, Mu-Ming P, Dan Y. Spike-timing-dependent synaptic plasticity depends on dendritic location. Nature. 2005 ; 434: 221-5
35. Gally IA, Montague PR, Reeke GN, Edelman GM. The NO hypothesis: possible effects of a short-lived, rapidly diffusible signal in the development and function of the nervous system. Proc Natl Acad Sci U S A. 1990 ; 87: 3547-51
36. Gjorgjieva J, Clopath C, Audet J, Pfister JP. A triplet spike-timing-dependent plasticity model generalizes the Bienenstock-Cooper-Munro rule to higher-order spatiotemporal correlations. Proc Natl Acad Sci U S A. 2011 ; 108: 19383-8
37. Golding NL, Staff NP, Spruston N. Dendritic spikes as a mechanism for cooperative long-term potentiation. Nature. 2002 ; 418 (6895). 326-31
38. Haas JS, Nowotny T, Abarbanel HDI. Spike-timing-dependent plasticity of inhibitory synapses in the entorhinal cortex. J Neurophysiol. 2006 ; 96: 3305-13
39. Halassa MM, Fellin T, Takano H, Dong JH, Haydon PG. Synaptic islands defined by the territory of a single astrocyte. J Neurosci. 2007 ; 27 (24). 6473-7
40. Han EB, Heinemann SF. Distal dendritic inputs control neuronal activity by heterosynaptic potentiation of proximal inputs. J Neurosci. 2013 ; 33: 1314-25
41. Hardingham N, Dachtler J, Fox K. The role of nitric oxide in pre-synaptic plasticity and homeostasis. Front Cell Neurosci. 2013 ; 7: 190
42. Hardingham NR, Hardingham GF, Fox KD, Jack JB. Presynaptic efficacy directs normalization of synaptic strength in layer 2/3 rat neocortex after paired activity. J Neurophysiol. 2007 ; 97: 2965-75
43. Hebb DO The organisation of behavior. New York, NY: Wiley ; 1949 :
44. Hölscher C, Anwyl R, Rowan MJ. Stimulation on the positive phase of hippocampal theta rhythm induces long-term potentiation that can be depotentiated by stimulation on the negative phase in area CA1 in vivo. J Neurosci. 1997 ; 17 (16). 6470-7
45. Huang Y, Yasuda H, Sarihi A, Tsumoto T. Roles of endocannabinoids in heterosynaptic long-term depression of excitatory synaptic transmission in visual cortex of young mice. J Neurosci. 2008 ; 28 (28). 7074-83
46. Kampa BM, Letzkus JJ, Stuart GJ. Requirement of dendritic calcium spikes for induction of spike-timing-dependent synaptic plasticity. J Physiol. 2006 ; 574 (1). 283-90
47. Kempter R, Gerstner W, van Hemmen JL. Intrinsic stabilization of output rates by spike-based Hebbian learning. Neural Comp. 2001 ; 13: 2709-41
48. Kossel A, Bonhoeffer T, Bolz J. Non-Hebbian synapses in rat visual cortex. Neuroreport. 1990 ; 1: 115-8
49. Kuhnt U, Voronin L. Interaction between paired-pulse facilitation and long-term potentiation in area CA1 of guinea-pig hippocampal slices: application of quantal analysis. Neuroscience. 1994 ; 62: 391-7
50. Lange MD, Doengi M, Lesting J, Pape HC, Jüngling K. Heterosynaptic long-term potentiation at interneuron-principal neuron synapses in the amygdala requires nitric oxide signalling. J Physiol. 2012 ; 590 (1). 131-43
51. Larkum ME, Kaiser KMM, Sakmann B. Calcium electrogenesis in distal apical dendrites of layer 5 pyramidal cells at a critical frequency of back-propagating action potentials. Proc Natl Acad Sci U S A. 1999 ; 96 (25). 14600-4
52. Lee CM, Stoelzel C, Chistiakova M, Volgushev M. Heterosynaptic plasticity induced by intracellular tetanization in layer 2/3 pyramidal neurons in rat auditory cortex. J Physiol. 2012 ; 590 (10). 2253-71
53. Letzkus JJ, Kampa BM, Stuart GJ. Learning rules for spike timing-dependent plasticity depend on dendritic synapse location. J Neurosci. 2006 ; 26: 10420-9
54. Lisman J, Spruston N. Postsynaptic depolarization requirements for LTP and LTD: a critique of spike timing-dependent plasticity. Nat Neurosci. 2005 ; 8 (7). 839-41
55. Lovatt D, Xu Q, Liu W, Takano T, Smith NA, Schnermann J. Neuronal adenosine release, and not astrocytic ATP release, mediates feedback inhibition of excitatory activity. Proc Natl Acad Sci. 2012 ; 109: 6265-70
56. Lynch GS, Dunwiddie T, Gribkoff V. Heterosynaptic depression: a postsynaptic correlate of long-term potentiation. Nature. 1977 ; 266: 737-9
57. Maejima T, Hashimoto K, Yoshida T, Aiba A, Kano M. Presynaptic inhibition caused by retrograde signal from metabotropic glutamate to cannabinoid receptors. Neuron. 2001 ; 31 (3). 463-75
58. Magee JC, Johnston D. A synaptically controlled, associative signal for Hebbian plasticity in hippocampal neurons. Science. 1997 ; 275 (5297). 209-13
59. Markram H, Luebke J, Frotscher M, Sakmann B. Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science. 1997 ; 275: 213-5
60. Miller KD. Synaptic economics: competition and cooperation in synaptic plasticity. Neuron. 1996 ; 17: 371-4
61. Miller KD, MacKay DJC. The role of constraints in Hebbian learning. Neural Comput. 1993 ; 6: 100-26
62. Miyakawa H, Ross WH, Jaffe D, Callaway JC, Lasser-Ross N, Lisman JE. Synaptically activated increases in Ca2+ concentration in hippocampal CA1 pyramidal cells are primarily due to voltage-gated Ca2+ channels. Neuron. 1992 ; 9: 1163-73
63. Nagase T, Ito KI, Kato K, Kaneko K, Kohda K, Matsumoto M. Long-term potentiation and long-term depression in hippocampal CA1 neurons of mice lacking the IP3 type 1 receptor. Neuroscience. 2003 ; 117: 821-30
64. Nakamura T, Barbara JG, Nakamura K, Ross WN. Synergistic Release of Ca2+ from IP3 sensitive stores evoked by synaptic activation of mGluRs paired with backpropagating action potentials. Neuron. 1999 ; 24 (3). 727-37
65. Neveu D, Zucker RS. Long-lasting potentiation and depression without presynaptic activity. J Neurophysiol. 1996 ; 75: 2157-60
66. Nevian T, Sakmann B. Single spine Ca2+ signals evoked by coincident EPSPs and backpropagating action potentials in spiny stellate cells of layer 4 in the juvenile rat somatosensory barrel cortex. J Neurosci. 2006 ; 26: 11001-13
67. Nishiyama M, Hong K, Mikoshiba K, Poo M, Kato K. Calcium stores regulate the polarity and input specificity of synaptic modification. Nature. 2000 ; 408: 584-8
68. Nugent FS, Penick EC, Kauer JA. Opioids block long-term potentiation of inhibitory synapses. Nature. 2007 ; 446 (7139). 1086-90
69. O'Dell TJ, Alger BE. Single calcium channels in rat and guinea-pig hippocampal neurons. J Physiol. 1991 ; 436: 739-67
70. Oja E. A simplified neuron model as a principal component analyzer. J Math Biol. 1982 ; 15: 267-73
71. Pan B, Hillard CJ, Liu QS. Endocannabinoid signaling mediates cocaine-induced inhibitory synaptic plasticity in midbrain dopamine neurons. J Neurosci. 2008 ; 28 (6). 1385-97
72. Pascual O, Casper KB, Kubera C, Zhang J, Revilla-Sanchez R, Sul JY. Astrocytic purinergic signaling coordinates synaptic networks. Science. 2005 ; 310: 113-6
73. Petrozzino JJ, Connor JA. Dendritic Ca2+ accumulations and metabotropic glutamate receptor activation associated with an NMDA receptor-independent long-term potentiation in hippocampal CA1 neurons. Hippocampus. 1994 ; 4: 546-58
74. Pfister JP, Gerstner W. Triplets of spikes in a model of spike timing-dependent plasticity. J Neurosci. 2006 ; 26: 9673-82
75. Phillips KG, Hardingham NR, Fox K. Postsynaptic action potentials are required for nitric-oxide-dependent long-term potentiation in CA1 neurons of adult GluR1 knock-out and wild-type mice. J Neurosci. 2008 ; 28 (52). 14031-41
76. Pockett S, Brookes NH, Bindman LJ. Long-term depression at synapses in slices of rat hippocampus can be induced by bursts of postsynaptic activity. Exp Brain Res. 1990 ; 80: 196-200
77. Rabinowitch I, Segev I. Two opposing plasticity mechanisms pulling a single synapse. Trends Neurosci. 2008 ; 31: 377-83
78. Royer S, Paré D. Conservation of total synaptic weight through balanced synaptic depression and potentiation. Nature. 2003 ; 422: 518-22
79. Schiller J, Helmchen F, Sakmann B. Spatial profile of dendritic calcium transients evoked by action potentials in rat neocortical pyramidal neurones. J Physiol. 1995 ; 487 (3). 583-600
80. Schiller J, Schiller Y, Clapham DE. NMDA receptors amplify calcium influx into dendritic spines during associative pre- and postsynaptic activation. Nat Neurosci. 1998 ; 1 (2). 114-8
81. Schuman EM, Madison DV. Locally distributed synaptic potentiation in the hippocampus. Science. 1994 ; 263: 532-6
82. Serrano A, Haddjeri N, Lacaille JC, Robitaille R. GABAergic network activation of glial cells underlies hippocampal heterosynaptic depression. J Neurosci. 2006 ; 26 (20). 5370-82
83. Sjöström PJ, Häusser M. A cooperative switch determines the sign of synaptic plasticity in distal dendrites of neocortical pyramidal neurons. Neuron. 2006 ; 51 (2). 227-38
84. Sjöström PJ, Turrigiano GG, Nelson SB. Rate, timing, and cooperativity jointly determine cortical synaptic plasticity. Neuron. 2001 ; 32: 1149-64
85. Skorheim S, Lonjers P, Bazhenov M. A spiking network model of decision making employing rewarded STDP. Plos One. 2014 ;:
86. Spruston N, Schiller Y, Stuart G, Sakmann B. Activity-dependent action potential invasion and calcium influx into hippocampal CA1 dendrites. Science. 1995 ; 268 (5208). 297-300
87. Staubli UV, Ji ZX. The induction of homo- vs. heterosynaptic LTD in area CA1 of hippocampal slices from adult rats. Brain Res. 1996 ; 714 (1). 169-76
88. Turrigiano GG. The self-tuning neuron: synaptic scaling of excitatory synapses. Cell. 2008 ; 135: 422-35
89. Turrigiano GG, Leslie KR, Desai NS, Rutherford LC, Nelson SB. Activity-dependent scaling of quantal amplitude in neocortical neurons. Nature. 1998 ; 391: 892-6
90. Van Rossum MC, Bi GQ, Turrigiano GG. Stable Hebbian learning from spike timing-dependent plasticity. J Neurosci. 2000 ; 20: 8812-21
91. Vitureira N, Letellier M, Goda Y. Homeostatic synaptic plasticity: from single synapses to neural circuits. Curr Opin Neurobiol. 2012 ; 22: 516-21
92. Volgushev M, Chistiakova M, Balaban P, Eysel UT. Retrograde signalling with nitric oxide at neocortical synapses. Eur J Neurosci. 2000 ; 12: 4255-67
93. Volgushev M, Mittmann T, Chistiakova M, Balaban P, Eysel UT. Interaction between intracellular tetanization and pairing-induced long-term synaptic plasticity in the rat visual cortex. Neuroscience. 1999 ; 93: 1227-32
94. Volgushev M, Voronin LL, Chistiakova M, Singer W. Induction of LTP and LTD in visual cortex neurons by intracellular tetanization. NeuroReport. 1994 ; 5: 2069-72
95. Volgushev M, Voronin LL, Chistiakova M, Singer W. Relations between long-term synaptic modifications and paired-pulse interactions in the rat neocortex. Eur J Neurosci. 1997 ; 9: 1656-65
96. Von der Malsburg C. Self-organization of orientation sensitive cells in the striate cortex. Kybernetik. 1973 ; 14: 85-100
97. Watt AJ, Sjöström PJ, Häusser M, Nelson SB, Turrigiano GG. A proportional but slower NMDA potentiation follows AMPA potentiation in LTP. Nat Neurosci. 2004 ; 7: 518-24
98. White G, Levy WB, Steward O. Spatial overlap between populations of synapses determines the extent of their associative interaction during the induction of long-term potentiation and depression. J Neurophysiol. 1990 ; 64 (4). 1186-98
99. Wöhrl R, von Haebler D, Heinemann U. Low-frequency stimulation of the direct cortical input to area CA1 induces homosynaptic LTD and heterosynaptic LTP in the rat hippocampal-entorhinal cortex slice preparation. Eur J Neurosci. 2007 ; 25 (1). 251-8
100. Wu Z, Yamaguchi Y. Conserving total synaptic weight ensures one-trial sequence learning of place fields in the hippocampus. Neural Networks. 2006 ; 19: 547-63
101. Yang SN, Tang YG, Zucker RS. Selective induction of LTP and LTD by postsynaptic [Ca2+]i elevation. J Neurophysiol. 1999 ; 81: 781-7
102. Yang Y, Calakos N. Presynaptic long-term plasticity. Front Synaptic Neurosci. 2013 ; 5: 8
103. Yasuda H, Huang Y, Tsumoto T. Regulation of excitability and plasticity by endocannabinoids and PKA in developing hippocampus. Proc Natl Acad Sci. 2008 ; 105 (8). 3106-11
104. Yeung LC, Shouval HZ, Blais BS, Cooper LN. Synaptic homeostasis and input selectivity follow from a calcium-dependent plasticity model. Proc Natl Acad Sci U S A. 2004 ; 101: 14943-8
105. Yuste R, Denk W. Dendritic spines as basic functional units of neuronal integration. Nature. 1995 ; 375: 682-4
106. Zenke F, Hennequin G, Gerstner W. Synaptic plasticity in neural networks needs homeostasis with a fast rate detector. PLoS Comput Biol. 2013 ; 9: e1003330
107. Zhang W, Linden DJ. The other side of the engram: experience-driven changes in neuronal intrinsic excitability. Nat Rev Neurosci. 2003 ; 4: 885-900
108. Zhang JM, Wang HK, Ye CQ, Ge W, Chen Y, Jiang ZL. ATP released by astrocytes mediates glutamatergic activity-dependent heterosynaptic suppression. Neuron. 2003 ; 40 (5). 971-82
109. Zhou YD, Acker CD, Netoff TI, Sen K, White JA. Increasing Ca2+ transients by broadening postsynaptic action potentials enhances timing-dependent synaptic depression. Proc Natl Acad Sci U S A. 2005 ; 102: 19121-5