Remodeling sensory cortical maps implants specific behavioral memory

Neuroscience

Volumn 246, Issue , 2013, Pages 40-51

  Bieszczad, K M ^a   Miasnikov, A A ^a   Weinberger, N M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Acetylcholine; Auditory cortex; Brain stimulation; Neurophysiology; Nucleus basalis

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; AUDITORY STIMULATION; BASAL AMYGDALA; BEHAVIOR; BRAIN DEPTH STIMULATION; CONTROLLED STUDY; IMPLANT; MALE; MEMORY; MEMORY CONSOLIDATION; MENTAL DEVELOPMENT; NERVE CELL PLASTICITY; NONHUMAN; PRIMARY AUDITORY CORTEX; PRIORITY JOURNAL; RAT; STATE DEPENDENT LEARNING;

ACOUSTIC STIMULATION; ANIMALS; AUDITORY CORTEX; BRAIN MAPPING; MALE; MEMORY; NEURONAL PLASTICITY; RANDOM ALLOCATION; RATS; RATS, SPRAGUE-DAWLEY; RESPIRATORY MECHANICS;

EID: 84878374466     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2013.04.038     Document Type: Article

References (69)

1. 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 USA 1996, 93:11219-11224.
2. Bandyopadhyay S., Shamma S.A., Kanold P.O. Dichotomy of functional organization in the mouse auditory cortex. Nat Neurosci 2010, 13:361-368.
3. Bao S., Chang E.F., Davis J.D., Gobeske K.T., Merzenich M.M. Progressive degradation and subsequent refinement of acoustic representations in the adult auditory cortex. J Neurosci 2003, 23:10765-10775.
4. Berlau K.M., Weinberger N.M. Learning strategy determines auditory cortical plasticity. Neurobiol Learn Mem 2008, 89:153-219.
5. Bieszczad K.M., Weinberger N.M. Remodeling the cortex in memory: increased use of a learning strategy increases the representational area of relevant acoustic cues. Neurobiol Learn Mem 2010, 94:127-171.
6. Bieszczad K.M., Weinberger N.M. Learning strategy trumps motivational level in determining learning-induced auditory cortical plasticity. Neurobiol Learn Mem 2010, 93:229-268.
7. Bieszczad K.M., Weinberger N.M. Representational gain in cortical area underlies increase of memory strength. Proc Natl Acad Sci USA 2010, 107:3793-3798.
8. Bieszczad K.M., Weinberger N.M. Extinction reveals that primary sensory cortex predicts reinforcement outcome. Eur J Neurosci 2012, 35:598-613.
9. Butt A.E., Chavez C.M., Flesher M.M., Kinney-Hurd B.L., Araujo G.C., Miasnikov A.A., Weinberger N.M. Association learning-dependent increases in acetylcholine release in the rat auditory cortex during auditory classical conditioning. Neurobiol Learn Mem 2009, 92:400-409.
10. Chen G., Yan J. Cholinergic modulation incorporated with a tone presentation induces frequency-specific threshold decreases in the auditory cortex of the mouse. Eur J Neurosci 2007, 25:1793-2596.
11. Diamond M.E., Petersen R.S., Harris J.A. Learning through maps: functional significance of topographic organization in primary sensory cortex. J Neurobiol 1999, 41:64-68.
12. Edeline J.M., Weinberger N.M. Thalamic short-term plasticity in the auditory system: associative retuning of receptive fields in the ventral medial geniculate body. Behav Neurosci 1991, 105:618-639.
13. Edeline J.M., Weinberger N.M. Receptive field plasticity in the auditory cortex during frequency discrimination training: selective retuning independent of task difficulty. Behav Neurosci 1993, 107:82-103.
14. Edeline J.M., Weinberger N.M. Non-awaking basal forebrain stimulation enhances auditory cortex responsiveness during slow-wave-sleep. Brain Res 1994, 636:333-337.
15. Engineer N.D., Riley J.R., Seale J.D., Vrana W.A., Shetake J.A., Sudanagunta S.P., Borland M.S., Kilgard M.P. Reversing pathological neural activity using targeted plasticity. Nature 2011, 470:101-104.
16. Engineer N.D., Møller A.R., Kilgard M.P. Directing neural plasticity to understand and treat tinnitus. Hear Res 2012, 1-9.
17. Fritz J., Shamma S., Elhilali M., Klein D. Rapid task-related plasticity of spectrotemporal receptive fields in primary auditory cortex. Nat Neurosci 2003, 6:1216-1223.
18. Froemke R.C., Merzenich M.M., Schreiner C.E. A synaptic memory trace for cortical receptive field plasticity. Nature 2007, 450:425-429.
19. Froemke R.C., Carcea I., Barker A.J., Yuan K., Seybold B.A., Martins A.R.O., Zaika N., Bernstein H., Wachs M., Levis P.A., Polley D.B., Merzenich M.M., Schreiner C.E. Long-term modification of cortical synapses improves sensory perception. Nat Neurosci 2013, 16(1):79-88.
20. Gilbert C.D., Wiesel T.N. Receptive field dynamics in adult primary visual cortex. Nature 1992, 356:150-152.
21. Goard M., Dan Y. Basal forebrain activation enhances cortical coding of natural scenes. Nat Neurosci 2009, 12:1444-1449.
22. Gonzalez-Lima F., Scheich H. Neural substrates for tone-conditioned bradycardia demonstrated with 2-deoxyglucose. II. Auditory cortex plasticity. Behav Brain Res 1986, 20:281-374.
23. Guo W., Chambers A.R., Darrow K.N., Hancock K.E., Shinn-Cunningham B.G., Polley D.B. Robustness of cortical topography across fields, laminae, anesthetic states, and neurophysiological signal types. J Neurosci 2012, 32:9159-9172.
24. Guo F., Intskirveli I., Blake D.T., Metherate R. Tone-detection training enhances spectral integration mediated by intracortical pathways in primary auditory cortex. Neurobiol Learn Mem 2013, 101:75-84.
25. Headley D.B., Weinberger N.M. Gamma-band activation predicts both associative memory and cortical plasticity. J Neurosci 2011, 31:12748-12758.
26. Headley D.B., Weinberger N.M. Fear conditioning enhances gamma oscillations and their entrainment of neurons representing the conditioned stimulus. J Neurosci 2013, 33:5705-5717.
27. Hui G.K., Wong K.L., Chavez C.M., Leon M.I., Robin K.M., Weinberger N.M. Conditioned tone control of brain reward behavior produces highly specific representational gain in the primary auditory cortex. Neurobiol Learn Mem 2009, 92:27-34.
28. James W. Habit 1890, H. Holt & Co., New York.
29. Jasper H.H., Tessier J. Acetylcholine liberation from cerebral cortex during paradoxical (REM) sleep. Science 1971, 172:601-602.
30. Ji W., Suga N. Development of reorganization of the auditory cortex caused by fear conditioning: effect of atropine. J Neurophysiol 2003, 90:1904-1909.
31. Kilgard M.P. Cortical map reorganization without cholinergic modulation. Neuron 2005, 48:529-530.
32. Kilgard M.P. Harnessing plasticity to understand learning and treat disease. TINS 2012, 35(12):715-722.
33. Kilgard M.P., Merzenich M.M. Cortical map reorganization enabled by nucleus basalis activity. Science 1998, 279:1714-1718.
34. Kisley M., Gerstein G. Daily variation and appetitive conditioning-induced plasticity of auditory cortex receptive fields. Eur J Neurosci 2001, 13:1993-3996.
35. Lozano A.M. Harnessing plasticity to reset dysfunctional neurons. N Engl J Med 2011, 364:1367-1368.
36. Martin S.J., Grimwood P.D., Morris R.G. Synaptic plasticity and memory: an evaluation of the hypothesis. Annu Rev Neurosci 2000, 23:649-711.
37. McLin D.E., Miasnikov A.A., Weinberger N.M. Induction of behavioral associative memory by stimulation of the nucleus basalis. Proc Natl Acad Sci USA 2002, 99:4002-4007.
38. McLin D.E., Miasnikov A.A., Weinberger N.M. CS-specific gamma, theta, and alpha EEG activity detected in stimulus generalization following induction of behavioral memory by stimulation of the nucleus basalis. Neurobiol Learn Mem 2003, 79:152-176.
39. Miasnikov A.A., Weinberger N.M. Detection of an inhibitory cortical gradient underlying peak shift in learning: a neural basis for a false memory. Neurobiol Learn Mem 2012, 98:368-379.
40. Miasnikov A.A., McLin D.E., Weinberger N.M. Muscarinic dependence of nucleus basalis induced conditioned receptive field plasticity. NeuroReport 2001, 12:1537-1542.
41. Miasnikov A.A., Chen J.C., Weinberger N.M. Rapid induction of specific associative behavioral memory by stimulation of the nucleus basalis in the rat. Neurobiol Learn Mem 2006, 86:47-65.
42. Miasnikov A.A., Chen J.C., Weinberger N.M. Specific auditory memory induced by nucleus basalis stimulation depends on intrinsic acetylcholine. Neurobiol Learn Mem 2008, 90:443-454.
43. Miasnikov A.A., Chen J.C., Gross N., Poytress B.S., Weinberger N.M. Motivationally neutral stimulation of the nucleus basalis induces specific behavioral memory. Neurobiol Learn Mem 2008, 90:125-137.
44. Miasnikov A.A., Chen J.C., Weinberger N.M. Consolidation and long-term retention of an implanted behavioral memory. Neurobiol Learn Mem 2011, 95:286-295.
45. Mishkin M., Petrie H.L. Memories and Habits: some implications for the analysis of learning and retention. Neuropsychology of memory 1984, 287-296. Guilford, New York, NY.
46. Mostofsky D.I. Stimulus generalization 1965, Boston University.
47. Ohl F., Scheich H. Learning-induced plasticity in animal and human auditory cortex. Curr Opin Neurobiol 2005, 15:470-477.
48. Ohl F., Scheich H., Freeman W. Change in pattern of ongoing cortical activity with auditory category learning. Nature 2001, 412:733-739.
49. Polley D., Steinberg E., Merzenich M. Perceptual learning directs auditory cortical map reorganization through top-down influences. J Neurosci 2006, 26:4970-5052.
50. Polley D., Read H., Storace D., Merzenich M. Multiparametric auditory receptive field organization across five cortical fields in the albino rat. J Neurophysiol 2007, 97:3621-3638.
51. Puckett A., Pandya P., Moucha R., Dai W., Kilgard M. Plasticity in the rat posterior auditory field following nucleus basalis stimulation. J Neurophysiol 2007, 98:253-265.
52. Recanzone G.H., Schreiner C.E., Merzenich M.M. Plasticity in the frequency representation of primary auditory cortex following discrimination training in adult owl monkeys. J Neurosci 1993, 13:87-103.
53. Reed A., Riley J., Carraway R., Carrasco A., Perez C., Jakkamsetti V., Kilgard M.P. Cortical map plasticity improves learning but is not necessary for improved performance. Neuron 2011, 70:121-131.
54. 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 USA 2005, 102:13664-13669.
55. Scheich H., Brechmann A., Brosch M., Budinger E., Ohl F., Selezneva E., Stark H., Tischmeyer W., Wetzel W. Behavioral semantics of learning and crossmodal processing in auditory cortex: the semantic processor concept. Hear Res 2011, 271:3-18.
56. Shepard K.N., Kilgard M.P., Liu R.C. Experience-dependent plasticity and auditory cortex. Springer handbook of auditory research 2012, 309-315. Springer, New York, NY.
57. Sherrington C.S. Experiments on the value of vascular and visceral factors for the genesis of emotion. Proc R Soc London 1900, 66:390-403.
58. Squire L.R., Stark C.E., Clark R.E. The medial temporal lobe. Annu Rev Neurosci 2004, 27:279-306.
59. Super H. Cognitive processes in the primary visual cortex: from perception to memory. Rev Neurosci 2002, 13:287-298.
60. Takahashi H., Funamizu A., Mitsumori Y., Kose H., Kanzaki R. Progressive plasticity of auditory cortex during appetitive operant conditioning. BioSystems 2010, 101:37-41.
61. Weinberger N.M. Dynamic regulation of receptive fields and maps in the adult sensory cortex. Ann Rev Neurosci 1995, 18:129-158.
62. Weinberger N.M. Specific long-term memory traces in primary auditory cortex. Nat Rev Neurosci 2004, 5:279-290.
63. Weinberger N.M. Associative representational plasticity in the auditory cortex: a synthesis of two disciplines. Learn Mem 2007, 14:1-16.
64. Weinberger N.M. Reconceptualizing the primary auditory cortex: learning, memory and specific plasticity. The auditory cortex 2011, 465-491. Springer, New York. J. Winer, C.E. Schreiner (Eds.).
65. Weinberger N.M., Javid R., Lepan B. Long-term retention of learning-induced receptive-field plasticity in the auditory cortex. Proc Natl Acad Sci USA 1993, 90:2394-2398.
66. Weinberger N.M., Miasnikov A.A., Chen J. The level of cholinergic nucleus basalis activation controls the specificity of auditory associative memory. Neurobiol Learn Mem 2006, 86:270-285.
67. Yan J., Zhang Y. Sound-guided shaping of the receptive field in the mouse auditory cortex by basal forebrain stimulation. Eur J Neurosci 2005, 21:563-576.
68. 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, 18:1521-1528.
69. Zhang Y., Hamilton S.E., Nathanson N.M., Yan J. Decreased input-specific plasticity of the auditory cortex in mice lacking M1 muscarinic acetylcholine receptors. Cereb Cortex 2006, 16:1258-1265.