Harnessing plasticity to understand learning and treat disease

Trends in Neurosciences

Volumn 35, Issue 12, 2012, Pages 715-722

  Kilgard, Michael P ^a  

^a UNIVERSITY OF TEXAS AT DALLAS   (United States)

Author keywords

Neuromodulation; Neuropathology; Rehabilitation; Sparse coding; Tinnitus; Vagus nerve stimulation

Indexed keywords

ACETYLCHOLINE; ACTIVITY REGULATED CYTOSKELETON ASSOCIATED PROTEIN; BRAIN DERIVED NEUROTROPHIC FACTOR; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NORADRENALIN; POSTSYNAPTIC DENSITY PROTEIN 95; SEROTONIN;

AMBLYOPIA; AUDITORY CORTEX; AUDITORY STIMULATION; BASAL AMYGDALA; BRAIN DAMAGE; CEREBROVASCULAR ACCIDENT; DISEASE ASSOCIATION; FOCAL DYSTONIA; GENE MUTATION; HUMAN; IN VIVO STUDY; LONG TERM DEPRESSION; NERVE CELL PLASTICITY; NEUROMUSCULAR ELECTRICAL STIMULATION; NONHUMAN; PHANTOM PAIN; PRIORITY JOURNAL; REPRODUCTIVE FITNESS; REVIEW; SENSORY CORTEX; SHAM PROCEDURE; TINNITUS; VAGUS NERVE STIMULATION;

ANIMALS; BRAIN; CENTRAL NERVOUS SYSTEM DISEASES; HUMANS; LEARNING; NEURONAL PLASTICITY;

EID: 84869865737     PISSN: 01662236     EISSN: 1878108X     Source Type: Journal    
DOI: 10.1016/j.tins.2012.09.002     Document Type: Review

References (114)

1. Olesen J., Leonardi M. The burden of brain diseases in Europe. Eur. J. Neurol. 2003, 10:471-477.
2. Møller A.R. Neural Plasticity and Disorders of the Nervous System 2006, Cambridge University Press.
3. Lozano A.M. Harnessing plasticity to reset dysfunctional neurons. N. Engl. J. Med. 2011, 364:1367-1368.
4. Latremoliere A., Woolf C.J. Central sensitization: a generator of pain hypersensitivity by central neural plasticity. J. Pain 2009, 10:895-926.
5. Buonomano D.V., Merzenich M.M. Cortical plasticity: from synapses to maps. Annu. Rev. Neurosci. 1998, 21:149-186.
6. Flor H., et al. Phantom-limb pain as a perceptual correlate of cortical reorganization following arm amputation. Nature 1995, 375:482-484.
7. Mühlnickel W., et al. Reorganization of auditory cortex in tinnitus. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:10340.
8. Langers D.R.M., et al. Tinnitus does not require macroscopic tonotopic map reorganization. Front. Syst. Neurosci. 2012, 6:2.
9. Engineer N.D., et al. Reversing pathological neural activity using targeted plasticity. Nature 2011, 470:101-104.
10. Bakin J.S., Weinberger N.M. 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.
11. Kilgard M.P., Merzenich M.M. Cortical map reorganization enabled by nucleus basalis activity. Science 1998, 279:1714-1718.
12. Reed A., et al. Cortical map plasticity improves learning but is not necessary for improved performance. Neuron 2011, 70:121-131.
13. Kilgard M.P., et al. Experience dependent plasticity alters cortical synchronization. Hear. Res. 2007, 229:171-179.
14. Puckett A.C., et al. Plasticity in the rat posterior auditory field following nucleus basalis stimulation. J. Neurophysiol. 2007, 98:253-265.
15. Pandya P.K., et al. Asynchronous inputs alter excitability, spike timing, and topography in primary auditory cortex. Hear. Res. 2005, 203:10-20.
16. Moucha R., et al. Background sounds contribute to spectrotemporal plasticity in primary auditory cortex. Exp. Brain Res. 2005, 162:417-427.
17. Kilgard M.P., et al. Spectral features control temporal plasticity in auditory cortex. Audiol. Neurootol. 2001, 6:196-202.
18. Kilgard M.P., Merzenich M.M. Plasticity of temporal information processing in the primary auditory cortex. Nat. Neurosci. 1998, 1:727-731.
19. Kilgard M.P., et al. Spectral features control temporal plasticity in auditory cortex. Audiol. Neurootol. 2001, 6:196-202.
20. Moucha R., Kilgard M.P. Cortical plasticity and rehabilitation. Prog. Brain Res. 2006, 157:111-122.
21. Hassert D., et al. The effects of peripheral vagal nerve stimulation at a memory-modulating intensity on norepinephrine output in the basolateral amygdala. Behav. Neurosci. 2004, 118:79.
22. Dorr A.E., Debonnel G. Effect of vagus nerve stimulation on serotonergic and noradrenergic transmission. J. Pharmacol. Exp. Ther. 2006, 318:890.
23. Nichols J.A., et al. Vagus nerve stimulation modulates cortical synchrony and excitability through the activation of muscarinic receptors. Neuroscience 2011, 189:207-214.
24. Clark K.B., et al. Enhanced recognition memory following vagus nerve stimulation in human subjects. Nat. Neurosci. 1999, 2:94-98.
25. Clark K., et al. Post-training unilateral vagal stimulation enhances retention performance in the rat. Neurobiol. Learn. Mem. 1995, 63:213-216.
26. Englot D.J., et al. Vagus nerve stimulation for epilepsy: a meta-analysis of efficacy and predictors of response. J. Neurosurg. 2011, 115:1248-1255.
27. Turner J.G., et al. Gap detection deficits in rats with tinnitus: a potential novel screening tool. Behav. Neurosci. 2006, 120:188.
28. Henry J.A., et al. General review of tinnitus: prevalence, mechanisms, effects, and management. J. Speech Lang. Hear. Res. 2005, 48:1204.
29. Eggermont J.J., Roberts L.E. The neuroscience of tinnitus. Trends Neurosci. 2004, 27:676-682.
30. Kilgard M.P., et al. Sensory input directs spatial and temporal plasticity in primary auditory cortex. J. Neurophysiol. 2001, 86:326.
31. Arns M., De Ridder D. Neurofeedback 2.0?. J. Neurother. 2011, 15:91-93.
32. Porter B.A., et al. Repeatedly pairing vagus nerve stimulation with a movement reorganizes primary motor cortex. Cereb. Cortex 2012, 22:2365-2367.
33. Skinner R., et al. Reduced sensory gating of the P1 potential in rape victims and combat veterans with posttraumatic stress disorder. Depress. Anxiety 1999, 9:122-130.
34. Davalos D.B., et al. Behavioral and electrophysiological indices of temporal processing dysfunction in schizophrenia. J. Neuropsychiatry Clin. Neurosci. 2005, 17:517-525.
35. Thomas C., et al. P50 gating deficit in Alzheimer dementia correlates to frontal neuropsychological function. Neurobiol. Aging 2010, 31:416-424.
36. Nagarajan S., et al. Cortical auditory signal processing in poor readers. Proc. Natl. Acad. Sci. U.S.A. 1999, 96:6483.
37. Shetake J., et al. Pairing tone trains with vagus nerve stimulation induces temporal plasticity in auditory cortex. Exp. Neurol. 2012, 342-349.
38. Zhang Y., Yan J. Corticothalamic feedback for sound-specific plasticity of auditory thalamic neurons elicited by tones paired with basal forebrain stimulation. Cereb. Cortex 2008, 18:1521.
39. Recanzone G., et al. Plasticity in the frequency representation of primary auditory cortex following discrimination training in adult owl monkeys. J. Neurosci. 1993, 13:87.
40. Recanzone G.H., et al. Topographic reorganization of the hand representation in cortical area 3b owl monkeys trained in a frequency-discrimination task. J. Neurophysiol. 1992, 67:1031.
41. Nudo R.J., et al. Use-dependent alterations of movement representations in primary motor cortex of adult squirrel monkeys. J. Neurosci. 1996, 16:785-807.
42. Kleim J.A., et al. Functional reorganization of the rat motor cortex following motor skill learning. J. Neurophysiol. 1998, 80:3321.
43. Rutkowski R.G., Weinberger N.M. 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.
44. Polley D.B., et al. Perceptual learning directs auditory cortical map reorganization through top-down influences. J. Neurosci. 2006, 26:4970.
45. Bieszczad K.M., Weinberger N.M. Representational gain in cortical area underlies increase of memory strength. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:3793.
46. Conner J.M., et al. Lesions of the basal forebrain cholinergic system impair task acquisition and abolish cortical plasticity associated with motor skill learning. Neuron 2003, 38:819-829.
47. Tzingounis A.V., Nicoll R.A. Arc/Arg3. 1: linking gene expression to synaptic plasticity and memory. Neuron 2006, 52:403-407.
48. Brennaman L.H., et al. Transgenic mice overexpressing the extracellular domain of NCAM are impaired in working memory and cortical plasticity. Neurobiol. Dis. 2011, 43:372-378.
49. Zhao M.G., et al. Roles of NMDA NR2B subtype receptor in prefrontal long-term potentiation and contextual fear memory. Neuron 2005, 47:859-872.
50. Mazarakis N.K., et al. Deficits in experience-dependent cortical plasticity and sensory-discrimination learning in presymptomatic Huntington's disease mice. J. Neurosci. 2005, 25:3059.
51. Glazewski S., et al. Requirement for α-CaMKII in experience-dependent plasticity of the barrel cortex. Science 1996, 272:421.
52. Edeline J.M. The thalamo-cortical auditory receptive fields: regulation by the states of vigilance, learning and the neuromodulatory systems. Exp. Brain Res. 2003, 153:554-572.
53. Thiel C.M. Pharmacological modulation of learning-induced plasticity in human auditory cortex. Restor. Neurol. Neurosci. 2007, 25:435-443.
54. Weinberger N.M. Reconceptualizing the primary auditory cortex: learning, memory and specific plasticity. The Auditory Cortex 2011, 465-491. Springer. J.A. Winer, C.E. Schreiner (Eds.).
55. Pilley J.W., Reid A.K. Border collie comprehends object names as verbal referents. Behav. Processes 2011, 86:184-195.
56. Been M., et al. Time-limited consolidation and task interference: no direct link. J. Neurosci. 2011, 31:14944-14951.
57. Lin C.H.J., et al. Interleaved practice enhances skill learning and the functional connectivity of fronto-parietal networks. Hum. Brain Mapp. 2012, 10.1002/hbm.22009.
58. Elbert T., et al. Alteration of digital representations in somatosensory cortex in focal hand dystonia. Neuroreport 1998, 9:3571.
59. Byl N.N., et al. A primate genesis model of focal dystonia and repetitive strain injury. Neurology 1996, 47:508.
60. Yang S., et al. Homeostatic plasticity drives tinnitus perception in an animal model. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:14974-14979.
61. Yotsumoto Y., et al. Different dynamics of performance and brain activation in the time course of perceptual learning. Neuron 2008, 57:827-833.
62. Yang G., et al. Stably maintained dendritic spines are associated with lifelong memories. Nature 2009, 462:920-924.
63. Ma L., et al. Changes in regional activity are accompanied with changes in inter-regional connectivity during 4 weeks motor learning. Brain Res. 2010, 1318:64-76.
64. Molina-Luna K., et al. Motor learning transiently changes cortical somatotopy. Neuroimage 2008, 40:1748-1754.
65. Takahashi H., et al. Learning-stage-dependent, field-specific, map plasticity in the rat auditory cortex during appetitive operant conditioning. Neuroscience 2011, 199:243-258.
66. Kato C., et al. Increased occlusal vertical dimension induces cortical plasticity in the rat face primary motor cortex. Behav. Brain Res. 2011, 228:254-260.
67. Hernández A., et al. Decoding a perceptual decision process across cortex. Neuron 2010, 66:300-314.
68. Lashley K.S. Mass action in cerebral function. Science 1931, 73:245-254.
69. Hodgson G.M. Darwinian coevolution of organizations and the environment. Ecol. Econ. 2010, 69:700-706.
70. Darwin C. On the Origin of Species by Means of Natural Selection, or, the Preservation of Favoured Races in the Struggle for Life 1907, John Murray.
71. Fernando C., et al. The neuronal replicator hypothesis. Neural Comput. 2010, 22:2809-2857.
72. Bandyopadhyay S., et al. Dichotomy of functional organization in the mouse auditory cortex. Nat. Neurosci. 2010, 13:361-368.
73. Watkins P.V., Barbour D.L. Level-tuned neurons in primary auditory cortex adapt differently to loud versus soft sounds. Cereb. Cortex 2011, 21:178.
74. Yin P., et al. Coding of amplitude modulation in primary auditory cortex. J. Neurophysiol. 2011, 105:582.
75. Brosch M., Schreiner C.E. Time course of forward masking tuning curves in cat primary auditory cortex. J. Neurophysiol. 1997, 77:923.
76. Sutter M.L., Schreiner C.E. Physiology and topography of neurons with multipeaked tuning curves in cat primary auditory cortex. J. Neurophysiol. 1991, 65:1207.
77. He J., et al. Temporal integration and duration tuning in the dorsal zone of cat auditory cortex. J. Neurosci. 1997, 17:2615.
78. Read H.L., et al. Functional architecture of auditory cortex. Curr. Opin. Neurobiol. 2002, 12:433-440.
79. Barbour D.L., Wang X. Auditory cortical responses elicited in awake primates by random spectrum stimuli. J. Neurosci. 2003, 23:7194.
80. Hromádka T., et al. Sparse representation of sounds in the unanesthetized auditory cortex. PLoS Biol. 2008, 6:e16.
81. Brosch M., et al. Representation of reward feedback in primate auditory cortex. Front. Syst. Neurosci. 2011, 5:5.
82. Otazu G.H., et al. Engaging in an auditory task suppresses responses in auditory cortex. Nat. Neurosci. 2009, 12:646-654.
83. Willmore B.D.B., et al. Sparse coding in striate and extrastriate visual cortex. J. Neurophysiol. 2011, 105:2907.
84. Finn I.M., Ferster D. Computational diversity in complex cells of cat primary visual cortex. J. Neurosci. 2007, 27:9638.
85. Sato T.R., Svoboda K. The functional properties of barrel cortex neurons projecting to the primary motor cortex. J. Neurosci. 2010, 30:4256.
86. Shamir M., Sompolinsky H. Implications of neuronal diversity on population coding. Neural Comput. 2006, 18:1951-1986.
87. Edelman G.M. Neural Darwinism: The Theory of Neuronal Group Selection 1987, Basic Books.
88. Crick F. Neural edelmanism. Trends Neurosci. 1989, 12:240-248.
89. De Ridder D., Van de Heyning P. The Darwinian plasticity hypothesis for tinnitus and pain. Prog. Brain Res. 2007, 166:55-60.
90. Bakin J.S., Weinberger N.M. Classical conditioning induces CS-specific receptive field plasticity in the auditory cortex of the guinea pig. Brain Res. 1990, 536:271-286.
91. Atiani S., et al. Task difficulty and performance induce diverse adaptive patterns in gain and shape of primary auditory cortical receptive fields. Neuron 2009, 61:467-480.
92. Kotaleski J.H., Blackwell K.T. Modelling the molecular mechanisms of synaptic plasticity using systems biology approaches. Nat. Rev. Neurosci. 2010, 11:239-251.
93. Shepherd J.D., Bear M.F. New views of Arc, a master regulator of synaptic plasticity. Nat. Neurosci. 2011, 14:279-284.
94. Silva A.J., et al. Molecular and cellular approaches to memory allocation in neural circuits. Science 2009, 326:391.
95. Song S., et al. Highly nonrandom features of synaptic connectivity in local cortical circuits. PLoS Biol. 2005, 3:e68.
96. Sáez I., Friedlander M.J. Plasticity between neuronal pairs in layer 4 of visual cortex varies with synapse state. J. Neurosci. 2009, 29:15286.
97. Fu M., et al. Repetitive motor learning induces coordinated formation of clustered dendritic spines in vivo. Nature 2012, 483:92-95.
98. Wolfe J., et al. Sparse and powerful cortical spikes. Curr. Opin. Neurobiol. 2010, 20:306-312.
99. Vogels T., et al. Inhibitory plasticity balances excitation and inhibition in sensory pathways and memory networks. Science 2011, 334:1569-1573.
100. Roelfsema P.R., et al. Perceptual learning rules based on reinforcers and attention. Trends Cogn. Sci. 2010, 14:64-71.
101. Buonomano D.V., Maass W. State-dependent computations: spatiotemporal processing in cortical networks. Nat. Rev. Neurosci. 2009, 10:113-125.
102. Engineer C.T., et al. Cortical activity patterns predict speech discrimination ability. Nat. Neurosci. 2008, 11:603.
103. Ranasinghe K., et al. neural mechanisms supporting robust discrimination of spectrally and temporally degraded speech. J. Assoc. Res. Otolaryngol. 2012, 13:527-542.
104. Pantev C., et al. Increased auditory cortical representation in musicians. Nature 1998, 392:811-814.
105. Han Y.K., et al. Early experience impairs perceptual discrimination. Nat. Neurosci. 2007, 10:1191-1197.
106. Bernstein J.G., Boyden E.S. Optogenetic tools for analyzing the neural circuits of behavior. Trends Cogn. Sci. 2011, 15:592-600.
107. Gdalyahu A., et al. Associative fear learning enhances sparse network coding in primary sensory cortex. Neuron 2012, 75:121-132.
108. Liu X., et al. Optogenetic stimulation of a hippocampal engram activates fear memory recall. Nature 2012, 484:381-385.
109. Nondahl D.M., et al. The ten-year incidence of tinnitus among older adults. Int. J. Audiol. 2010, 49:580-585.
110. Cramer S.C., et al. Harnessing neuroplasticity for clinical applications. Brain 2011, 134:1591.
111. Woloszyn L., Sheinberg D.L. Effects of long-term visual experience on responses of distinct classes of single units in inferior temporal cortex. Neuron 2012, 74:193-205.
112. Surowiecki J. The Wisdom of Crowds: Why the Many are Smarter than the Few and How Collective Wisdom Shapes Business, Economies, Societies, and Nations 2004, Doubleday Books.
113. Georgopoulos A.P., et al. Neuronal population coding of movement direction. Science 1986, 233:1416-1419.
114. Lai C.S.W., et al. Opposite effects of fear conditioning and extinction on dendritic spine remodelling. Nature 2012, 483:87-91.