Presynaptic gating of postsynaptic synaptic plasticity: A plasticity filter in the adult auditory cortex

Neuroscientist

Volumn 19, Issue 5, 2013, Pages 465-478

  Blundon, Jay A ^a   Zakharenko, Stanislav S ^a  

^a ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

adenosine; auditory cortex; perceptual memory; presynaptic; synaptic plasticity; thalamocortical synapses

Indexed keywords

AUDITORY CORTEX; BRAIN DEVELOPMENT; HUMAN; MODULATION; NERVE CELL NETWORK; NERVE CELL PLASTICITY; PRIORITY JOURNAL; REVIEW; SENSORY CORTEX; SENSORY GATING; THALAMOCORTICAL TRACT;

ADENOSINE; AUDITORY CORTEX; PERCEPTUAL MEMORY; PRESYNAPTIC; SYNAPTIC PLASTICITY; THALAMOCORTICAL SYNAPSES;

ANIMALS; AUDITORY CORTEX; AUDITORY PERCEPTION; HUMANS; LEARNING; NEURONAL PLASTICITY; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 84883727251     PISSN: 10738584     EISSN: 10894098     Source Type: Journal    
DOI: 10.1177/1073858413482983     Document Type: Review

References (98)

1. Abe K, Nakata A, Mizutani A, Saito H. Facilitatory but nonessential role of the muscarinic cholinergic system in the generation of long-term potentiation of population spikes in the dentate gyrus in vivo. Neuropharmacology. 1994 ; 33: 847-52
2. Amitai Y. Thalamocortical synaptic connections: efficacy, modulation, inhibition and plasticity. Rev Neurosci. 2001 ; 12: 159-73
3. Bakin JS, Weinberger NM. Classical conditioning induces CS-specific receptive field plasticity in the auditory cortex of the guinea pig. Brain Res. 1990 ; 536: 271-86
4. Bakin JS, Weinberger NM. Induction of a physiological memory in the cerebral cortex by stimulation of the nucleus basalis. Proc Natl Acad Sci U S A. 1996 ; 93: 11219-24
5. Bao S, Chan VT, Merzenich MM. Cortical remodelling induced by activity of ventral tegmental dopamine neurons. Nature. 2001 ; 412: 79-83
6. Barkat TR, Polley DB, Hensch TK. A critical period for auditory thalamocortical connectivity. Nat Neurosci. 2011 ; 14: 1189-94
7. Barth AL, Malenka RC. NMDAR EPSC kinetics do not regulate the critical period for LTP at thalamocortical synapses. Nat Neurosci. 2001 ; 4: 235-6
8. Bayazitov IT, Richardson RJ, Fricke RG, Zakharenko SS. Slow presynaptic and fast postsynaptic components of compound long-term potentiation. J Neurosci. 2007 ; 27: 11510-21
9. Bear MF, Singer W. Modulation of visual cortical plasticity by acetylcholine and noradrenaline. Nature. 1986 ; 320: 172-6
10. Bjordahl TS, Dimyan MA, Weinberger NM. Induction of long-term receptive field plasticity in the auditory cortex of the waking guinea pig by stimulation of the nucleus basalis. Behav Neurosci. 1998 ; 112: 467-79
11. Blake DT, Heiser MA, Caywood M, Merzenich MM. Experience-dependent adult cortical plasticity requires cognitive association between sensation and reward. Neuron. 2006 ; 52: 371-81
12. Blitzer RD, Gil O, Landau EM. Cholinergic stimulation enhances long-term potentiation in the CA1 region of rat hippocampus. Neurosci Lett. 1990 ; 119: 207-10
13. Blundon JA, Bayazitov IT, Zakharenko SS. Presynaptic gating of postsynaptically expressed plasticity at mature thalamocortical synapses. J Neurosci. 2011 ; 31: 16012-25
14. Blundon JA, Zakharenko SS. Dissecting the components of long-term potentiation. Neuroscientist. 2008 ; 14: 598-608
15. Bouron A, Reuter H. Muscarinic stimulation of synaptic activity by protein kinase C is inhibited by adenosine in cultured hippocampal neurons. Proc Natl Acad Sci U S A. 1997 ; 94: 12224-9
16. Boyden ES, Zhang F, Bamberg E, Nagel G, Deisseroth K. Millisecond-timescale, genetically targeted optical control of neural activity. Nat Neurosci. 2005 ; 8: 1263-8
17. Brocher S, Artola A, Singer W. Agonists of cholinergic and noradrenergic receptors facilitate synergistically the induction of long-term potentiation in slices of rat visual cortex. Brain Res. 1992 ; 573: 27-36
18. Castro-Alamancos MA. Short-term plasticity in thalamocortical pathways: cellular mechanisms and functional roles. Rev Neurosci. 1997 ; 8: 95-116
19. Castro-Alamancos MA, Connors BW. Short-term synaptic enhancement and long-term potentiation in neocortex. Proc Natl Acad Sci U S A. 1996 ; 93: 1335-9
20. Chowdhury SA, Suga N. Reorganization of the frequency map of the auditory cortex evoked by cortical electrical stimulation in the big brown bat. J Neurophysiol. 2000 ; 83: 1856-63
21. Chun SK, Bayazitov IT, Blundon JA, Zakharenko SS. Thalamocortical LTP becomes gated after the early critical period in the auditory cortex. J Neurosci. 2013 ;:
22. Cooke SF, Bear MF. Visual experience induces long-term potentiation in the primary visual cortex. J Neurosci. 2010 ; 30: 16304-13
23. Crair MC, Malenka RC. A critical period for long-term potentiation at thalamocortical synapses. Nature. 1995 ; 375: 325-8
24. de Villers-Sidani E, Chang EF, Bao S, Merzenich MM. Critical period window for spectral tuning defined in the primary auditory cortex (A1) in the rat. J Neurosci. 2007 ; 27: 180-9
25. Diamond DM, Weinberger NM. Classical conditioning rapidly induces specific changes in frequency receptive fields of single neurons in secondary and ventral ectosylvian auditory cortical fields. Brain Res. 1986 ; 372: 357-60
26. Dudek SM, Friedlander MJ. Developmental down-regulation of LTD in cortical layer IV and its independence of modulation by inhibition. Neuron. 1996 ; 16: 1097-106
27. Dunwiddie TV, Fredholm BB. Adenosine A1 receptors inhibit adenylate cyclase activity and neurotransmitter release and hyperpolarize pyramidal neurons in rat hippocampus. J Pharmacol Exp Ther. 1989 ; 249: 31-7
28. Dunwiddie TV, Masino SA. The role and regulation of adenosine in the central nervous system. Annu Rev Neurosci. 2001 ; 24: 31-55
29. Edeline JM, Hars B, Maho C, Hennevin E. Transient and prolonged facilitation of tone-evoked responses induced by basal forebrain stimulations in the rat auditory cortex. Exp Brain Res. 1994 ; 97: 373-86
30. Edeline JM, Manunta Y, Hennevin E. Induction of selective plasticity in the frequency tuning of auditory cortex and auditory thalamus neurons by locus coeruleus stimulation. Hear Res. 2011 ; 274: 75-84
31. Ehret G. Development of absolute auditory thresholds in the house mouse (Mus musculus). J Am Audiol Soc. 1976 ; 1: 179-84
32. Feldman DE, Nicoll RA, Malenka RC. Synaptic plasticity at thalamocortical synapses in developing rat somatosensory cortex: LTP, LTD, and silent synapses.. J Neurobiol. 1999 ; 41: 92-101
33. Feldman DE, Nicoll RA, Malenka RC, Isaac JT. Long-term depression at thalamocortical synapses in developing rat somatosensory cortex. Neuron. 1998 ; 21: 347-57
34. Fritz JB, Elhilali M, David SV, Shamma SA. Does attention play a role in dynamic receptive field adaptation to changing acoustic salience in A1?. Hear Res. 2007 ; 229: 186-203
35. Froemke RC, Merzenich MM, Schreiner CE. A synaptic memory trace for cortical receptive field plasticity. Nature. 2007 ; 450: 425-9
36. Gagolewicz PJ, Dringenberg HC. NR2B-subunit dependent facilitation of long-term potentiation in primary visual cortex following visual discrimination training of adult rats. Eur J Neurosci. 2011 ; 34: 1222-9
37. Gao E, Suga N. Experience-dependent corticofugal adjustment of midbrain frequency map in bat auditory system. Proc Natl Acad Sci U S A. 1998 ; 95: 12663-70
38. Gao E, Suga N. Experience-dependent plasticity in the auditory cortex and the inferior colliculus of bats: role of the corticofugal system. Proc Natl Acad Sci U S A. 2000 ; 97: 8081-6
39. Gil Z, Connors BW, Amitai Y. Differential regulation of neocortical synapses by neuromodulators and activity. Neuron. 1997 ; 19: 679-86
40. Gil Z, Connors BW, Amitai Y. Efficacy of thalamocortical and intracortical synaptic connections: quanta, innervation, and reliability. Neuron. 1999 ; 23: 385-97
41. Gordon B, Mitchell B, Mohtadi K, Roth E, Tseng Y, Turk F. Lesions of nonvisual inputs affect plasticity, norepinephrine content, and acetylcholine content of visual cortex. J Neurophysiol. 1990 ; 64: 1851-60
42. Gu Q, Singer W. Effects of intracortical infusion of anticholinergic drugs on neuronal plasticity in kitten striate cortex. Eur J Neurosci. 1993 ; 5: 475-85
43. Hars B, Maho C, Edeline JM, Hennevin E. Basal forebrain stimulation facilitates tone-evoked responses in the auditory cortex of awake rat. Neuroscience. 1993 ; 56: 61-74
44. Heynen AJ, Bear MF. Long-term potentiation of thalamocortical transmission in the adult visual cortex in vivo. J Neurosci. 2001 ; 21: 9801-13
45. Hogsden JL, Dringenberg HC. Decline of long-term potentiation (LTP) in the rat auditory cortex in vivo during postnatal life: involvement of NR2B subunits. Brain Res. 2009a ; 1283: 25-33
46. Hogsden JL, Dringenberg HC. NR2B subunit-dependent long-term potentiation enhancement in the rat cortical auditory system in vivo following masking of patterned auditory input by white noise exposure during early postnatal life. Eur J Neurosci. 2009b ; 30: 376-84
47. Hohmann CF, Berger-Sweeney J. Cholinergic regulation of cortical development and plasticity. New twists to an old story. Perspect Dev Neurobiol. 1998 ; 5: 401-25
48. Huang S, Trevino M, He K, Ardiles A, Pasquale R, Guo Y. Pull-push neuromodulation of LTP and LTD enables bidirectional experience-induced synaptic scaling in visual cortex. Neuron. 2012 ; 73: 497-510
49. Insanally MN, Kover H, Kim H, Bao S. Feature-dependent sensitive periods in the development of complex sound representation. J Neurosci. 2009 ; 29: 5456-62
50. Ji W, Suga N. Development of reorganization of the auditory cortex caused by fear conditioning: effect of atropine. J Neurophysiol. 2003 ; 90: 1904-9
51. Ji W, Suga N, Gao E. Effects of agonists and antagonists of NMDA and ACh receptors on plasticity of bat auditory system elicited by fear conditioning. J Neurophysiol. 2005 ; 94: 1199-211
52. Jiang B, Trevino M, Kirkwood A. Sequential development of long-term potentiation and depression in different layers of the mouse visual cortex. J Neurosci. 2007 ; 27: 9648-52
53. Juliano SL, Ma W, Bear MF, Eslin D. Cholinergic manipulation alters stimulus-evoked metabolic activity in cat somatosensory cortex. J Comp Neurol. 1990 ; 297: 106-20
54. Kato N, Artola A, Singer W. Developmental changes in the susceptibility to long-term potentiation of neurones in rat visual cortex slices. Brain Res Dev Brain Res. 1991 ; 60: 43-50
55. Keuroghlian AS, Knudsen EI. Adaptive auditory plasticity in developing and adult animals. Prog Neurobiol. 2007 ; 82: 109-21
56. Kilgard MP, Merzenich MM. Cortical map reorganization enabled by nucleus basalis activity. Science. 1998a ; 279: 1714-8
57. Kilgard MP, Merzenich MM. Plasticity of temporal information processing in the primary auditory cortex. Nat Neurosci. 1998b ; 1: 727-31
58. King AJ, Nelken I. Unraveling the principles of auditory cortical processing: can we learn from the visual system?. Nat Neurosci. 2009 ; 12: 698-701
59. Kirkwood A, Bear MF. Hebbian synapses in visual cortex. J Neurosci. 1994a ; 14: 1634-45
60. Kirkwood A, Bear MF. Homosynaptic long-term depression in the visual cortex. J Neurosci. 1994b ; 14: 3404-12
61. Kirkwood A, Lee HK, Bear MF. Co-regulation of long-term potentiation and experience-dependent synaptic plasticity in visual cortex by age and experience. Nature. 1995 ; 375: 328-31
62. Kraus HJ, Aulbach-Kraus K. Morphological changes in the cochlea of the mouse after the onset of hearing. Hear Res. 1981 ; 4: 89-102
63. Kumar A. Carbachol-induced long-term synaptic depression is enhanced during senescence at hippocampal CA3-CA1 synapses. J Neurophysiol. 2010 ; 104: 607-16
64. Lee SM, Ebner FF. Induction of high frequency activity in the somatosensory thalamus of rats in vivo results in long-term potentiation of responses in SI cortex. Exp Brain Res. 1992 ; 90: 253-61
65. Ma X, Suga N. Augmentation of plasticity of the central auditory system by the basal forebrain and/or somatosensory cortex. J Neurophysiol. 2003 ; 89: 90-103
66. Ma X, Suga N. Long-term cortical plasticity evoked by electric stimulation and acetylcholine applied to the auditory cortex. Proc Natl Acad Sci U S A. 2005 ; 102: 9335-40
67. Maeda T, Kaneko S, Satoh M. Roles of endogenous cholinergic neurons in the induction of long-term potentiation at hippocampal mossy fiber synapses. Neurosci Res. 1994 ; 20: 71-8
68. McCutchen E, Scheiderer CL, Dobrunz LE, McMahon LL. Coexistence of muscarinic long-term depression with electrically induced long-term potentiation and depression at CA3-CA1 synapses. J Neurophysiol. 2006 ; 96: 3114-21
69. Mechawar N, Descarries L. The cholinergic innervation develops early and rapidly in the rat cerebral cortex: a quantitative immunocytochemical study. Neuroscience. 2001 ; 108: 555-67
70. Metherate R, Ashe JH. Nucleus basalis stimulation facilitates thalamocortical synaptic transmission in the rat auditory cortex. Synapse. 1993 ; 14: 132-43
71. Metherate R, Weinberger NM. Cholinergic modulation of responses to single tones produces tone-specific receptive field alterations in cat auditory cortex. Synapse. 1990 ; 6: 133-45
72. Miasnikov AA, McLin D, Weinberger NM. Muscarinic dependence of nucleus basalis induced conditioned receptive field plasticity. Neuroreport. 2001 ; 12: 1537-42
73. Molnar Z, Adams R, Blakemore C. Mechanisms underlying the early establishment of thalamocortical connections in the rat. J Neurosci. 1998 ; 18: 5723-45
74. Oliveira L, Timoteo MA, Correia-de-Sa P. Negative crosstalk between M1 and M2 muscarinic autoreceptors involves endogenous adenosine activating A1 receptors at the rat motor endplate. Neurosci Lett. 2009 ; 459: 127-31
75. Polley DB, Steinberg EE, Merzenich MM. Perceptual learning directs auditory cortical map reorganization through top-down influences. J Neurosci. 2006 ; 26: 4970-82
76. Recanzone GH, Schreiner CE, Merzenich MM. Plasticity in the frequency representation of primary auditory cortex following discrimination training in adult owl monkeys. J Neurosci. 1993 ; 13: 87-103
77. Richardson RJ, Blundon JA, Bayazitov IT, Zakharenko SS. Connectivity patterns revealed by mapping of active inputs on dendrites of thalamorecipient neurons in the auditory cortex. J Neurosci. 2009 ; 29: 6406-17
78. Robertson RT, Mostamand F, Kageyama GH, Gallardo KA, Yu J. Primary auditory cortex in the rat: transient expression of acetylcholinesterase activity in developing geniculocortical projections. Brain Res Dev Brain Res. 1991 ; 58: 81-95
79. Rutkowski RG, Weinberger NM. Encoding of learned importance of sound by magnitude of representational area in primary auditory cortex. Proc Natl Acad Sci U S A. 2005 ; 102: 13664-9
80. Sachdev RN, Lu SM, Wiley RG, Ebner FF. Role of the basal forebrain cholinergic projection in somatosensory cortical plasticity. J Neurophysiol. 1998 ; 79: 3216-28
81. Sally SL, Kelly JB. Organization of auditory cortex in the albino rat: sound frequency. J Neurophysiol. 1988 ; 59: 1627-38
82. Shatz CJ. Emergence of order in visual system development. Proc Natl Acad Sci U S A. 1996 ; 93: 602-8
83. Stratford KJ, Tarczy-Hornoch K, Martin KA, Bannister NJ, Jack JJ. Excitatory synaptic inputs to spiny stellate cells in cat visual cortex. Nature. 1996 ; 382: 258-61
84. Suga N, Ma X. Multiparametric corticofugal modulation and plasticity in the auditory system. Nat Rev Neurosci. 2003 ; 4: 783-94
85. Sun YJ, Wu GK, Liu BH, Li P, Zhou M, Xiao Z. Fine-tuning of pre-balanced excitation and inhibition during auditory cortical development. Nature. 2010 ; 465: 927-31
86. Thiel CM, Friston KJ, Dolan RJ. Cholinergic modulation of experience-dependent plasticity in human auditory cortex. Neuron. 2002 ; 35: 567-74
87. Weinberger NM. Physiological memory in primary auditory cortex: characteristics and mechanisms. Neurobiol Learn Mem. 1998 ; 70: 226-51
88. Weinberger NM. The nucleus basalis and memory codes: auditory cortical plasticity and the induction of specific, associative behavioral memory. Neurobiol Learn Mem. 2003 ; 80: 268-84
89. Weinberger NM. Specific long-term memory traces in primary auditory cortex. Nat Rev Neurosci. 2004 ; 5: 279-90
90. Weinberger NM. Associative representational plasticity in the auditory cortex: a synthesis of two disciplines. Learn Mem. 2007a ; 14: 1-16
91. Weinberger NM. Auditory associative memory and representational plasticity in the primary auditory cortex. Hear Res. 2007b ; 229: 54-68
92. Wiesel T, Hubel D. Comparison of the effects of unilateral and bilateral eye closure on cortical unit responses in kittens. J Neurophysiol. 1965 ; 28: 1029-40
93. Worley PF, Baraban JM, McCarren M, Snyder SH, Alger BE. Cholinergic phosphatidylinositol modulation of inhibitory, G protein-linked neurotransmitter actions: electrophysiological studies in rat hippocampus. Proc Natl Acad Sci U S A. 1987 ; 84: 3467-71
94. Yu X, Chung S, Chen DY, Wang S, Dodd SJ, Walters JR. Thalamocortical inputs show post-critical-period plasticity. Neuron. 2012 ; 74: 731-42
95. Zakharenko SS, Patterson SL, Dragatsis I, Zeitlin SO, Siegelbaum SA, Kandel ER. Presynaptic BDNF required for a presynaptic but not postsynaptic component of LTP at hippocampal CA1-CA3 synapses. Neuron. 2003 ; 39: 975-90
96. Zakharenko SS, Zablow L, Siegelbaum SA. Visualization of changes in presynaptic function during long-term synaptic plasticity. Nat Neurosci. 2001 ; 4: 711-7
97. Zhang LI, Bao S, Merzenich MM. Persistent and specific influences of early acoustic environments on primary auditory cortex. Nat Neurosci. 2001 ; 4: 1123-30
98. Zhang Y, Hamilton SE, Nathanson NM, Yan J. Decreased input-specific plasticity of the auditory cortex in mice lacking M1 muscarinic acetylcholine receptors. Cereb Cortex. 2006 ; 16: 1258-65