Sensory experience determines enrichment-induced plasticity in rat auditory cortex

Brain Research

Volumn 1174, Issue 1, 2007, Pages 76-91

  Percaccio, Cherie R ^a   Pruette, Autumn L ^a   Mistry, Shilpa T ^a   Chen, Yeting H ^a   Kilgard, Michael P ^a  

^a UNIVERSITY OF TEXAS AT DALLAS   (United States)

Author keywords

Acetylcholine; Nucleus basalis

Indexed keywords

ACETYLCHOLINE; IMMUNOGLOBULIN G; SAPORIN;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ARTICLE; AUDITORY CORTEX; AUDITORY STIMULATION; AUTISM; CHOLINERGIC SYSTEM; CONTROLLED STUDY; ENVIRONMENT; EVOKED RESPONSE; EXERCISE; FEMALE; NONHUMAN; OLIVARY NUCLEUS; PLASTICITY; PRIORITY JOURNAL; RAT; SCHIZOPHRENIA; SENSORY SYSTEM; WAKEFULNESS;

ACETYLCHOLINE; ACOUSTIC STIMULATION; ANIMALS; AUDITORY CORTEX; ELECTRODES, IMPLANTED; ENVIRONMENT; ENVIRONMENT DESIGN; FEMALE; NEURONAL PLASTICITY; PHYSICAL CONDITIONING, ANIMAL; RATS; RATS, SPRAGUE-DAWLEY; SOCIAL BEHAVIOR;

RATTUS;

EID: 34748821309     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2007.07.062     Document Type: Article

References (115)

1. Adler L.E., Olincy A., Waldo M., Harris J.G., Griffith J., Stevens K., Flach K., Nagamoto H., Bickford P., Leonard S., and Freedman R. Schizophrenia, sensory gating, and nicotinic receptors. Schizophr. Bull. 24 (1998) 189-202
2. Anderson B.J., Eckburg P.B., and Relucio K.I. Alterations in thickness of motor cortical subregions after motor skill learning and exercise. Learn. Mem. 9 (2002) 1-9
3. Bao S., Chang E.F., Davis J.D., Gobeske K.T., and Merzenich M.M. Progressive degradation and subsequent refinement of acoustic representations in the adult auditory cortex. J. Neurosci. 23 (2003) 10765-10775
4. Baptista L.F., and Gaunt S.L.L. Social interaction and vocal development. In: Snowdon C.T., and Hausberger M. (Eds). Social Influences on Vocal Development (1997), Cambridge University Press, Cambridge 23-41
5. Barth D.S., and Di S. Three-dimensional analysis of auditory-evoked potentials in rat neocortex. J. Neurophysiol. 64 (1990) 1527-1536
6. Baskerville K.A., Schweitzer J.B., and Herron P. Effects of cholinergic depletion on experience-dependent plasticity in the cortex of the rat. Neuroscience 80 (1997) 1159-1169
7. Bear M.F., and Singer W. Modulation of visual cortical plasticity by acetylcholine and noradrenaline. Nature 320 (1986) 172-176
8. Beaulieu C., and Cynader M. Effect of the richness of the environment on neurons in cat visual cortex. I. Receptive field properties. Brain Res. Dev. Brain Res. 53 (1990) 71-81
9. Beaulieu C., and Cynader M. Effect of the richness of the environment on neurons in cat visual cortex. II. Spatial and temporal frequency characteristics. Dev. Brain Res. 53 (1990) 82-88
10. Bennett E.L., Rosenzweig M.R., and Diamond M.C. Rat brain: effects of environmental enrichment on wet and dry weights. Science 163 (1969) 825-826
11. Bennett E.L., Krech D., and Rosenzweig M.R. Reliability and regional specificity of cerebral effects of environmental complexity and training. J. Comp. Physiol. Psychol. 57 (1964) 440-441
12. Berger-Sweeney J., Stearns N.A., Frick K.M., Beard B., and Baxter M.G. Cholinergic basal forebrain is critical for social transmission of food preferences. Hippocampus 10 (2000) 729-738
13. Black J.E., Isaacs K.R., Anderson B.J., Alcantara A.A., and Greenough W.T. Learning causes synaptogenesis, whereas motor activity causes angiogenesis, in cerebellar cortex of adult rats. Proc. Natl. Acad. Sci. U. S. A. 87 (1990) 5568-5572
14. Book A.A., Wiley R.G., and Schweitzer J.B. Specificity of 192 IgG-saporin for NGF receptor-positive cholinergic basal forebrain neurons in the rat. Brain Res. 590 (1992) 350-355
15. Braff D.L., and Geyer M.A. Sensorimotor gating and schizophrenia. Human and animal model studies. Arch. Gen. Psychiatry 47 (1990) 181-188
16. Buchwald J.S., Erwin R., Van Lancker D., Guthrie D., Schwafel J., and Tanguay P. Midlatency auditory evoked responses: P1 abnormalities in adult autistic subjects. Electroencephalogr. Clin. Neurophysiol. 84 (1992) 164-171
17. Casamenti F., Di Patre P.L., Bartolini L., and Pepeu G. Unilateral and bilateral nucleus basalis lesions: differences in neurochemical and behavioral recovery. Neuroscience 24 (1988) 209-215
18. Condon C.D., and Weinberger N.M. Habituation produces frequency-specific plasticity of receptive fields in the auditory cortex. Behav. Neurosci. 105 (1991) 416-430
19. Conner J.M., Culberson A., Packowski C., Chiba A.A., and Tuszynski M.H. Lesions of the basal forebrain cholinergic system impair task acquisition and abolish cortical plasticity associated with motor skill learning. Neuron 38 (2003) 819-829
20. Coq J.O., and Xerri C. Environmental enrichment alters organizational features of the forepaw representation in the primary somatosensory cortex of adult rats. Exp. Brain Res. 121 (1998) 191-204
21. Cullum C.M., Harris J.G., Waldo M.C., Smernoff E., Madison A., Nagamoto H.T., Griffith J.M., Adler L.E., and Freedman R. Neurophysiological and neuropsychological evidence for attentional dysfunction in schizophrenia. Schizophr. Res. 10 (1993) 131-141
22. de Castro J.M., and Duncan G. Operantly conditioned running: effects on brain catecholamine concentrations and receptor densities in the rat. Pharmacol. Biochem. Behav. 23 (1985) 495-500
23. Delacour J., Houcine O., and Costa J.C. Evidence for a cholinergic mechanism of "learned" changes in the responses of barrel field neurons of the awake and undrugged rat. Neuroscience 34 (1990) 1-8
24. Devenport L., Dallas S., Carpenter C., and Renner M.J. The relationship between adrenal steroids and enrichment-induced brain growth. Behav. Neural Biol. 58 (1992) 48-50
25. Diamond M.C. Response of the brain to enrichment. An. Acad. Bras. Cienc. 73 (2001) 211-220
26. Diamond M.C., Law F., Rhodes H., Lindner B., Rosenzweig M.R., Krech D., and Bennett E.L. Increases in cortical depth and glia numbers in rats subjected to enriched environment. J. Comp. Neurol. 128 (1966) 117-126
27. Dinse H.R., Kleibel N., Kalisch T., Ragert P., Wilimzig C., and Tegenthoff M. Tactile coactivation resets age-related decline of human tactile discrimination. Ann. Neurol. 60 (2006) 88-94
28. Einon D.F., Humphreys A.P., Chivers S.M., Field S., and Naylor V. Isolation has permanent effects upon the behavior of the rat, but not the mouse, gerbil, or guinea pig. Dev. Psychobiol. 14 (1981) 343-355
29. Engineer N.D., Percaccio C.R., Pandya P.K., Moucha R., Rathbun D.L., and Kilgard M.P. Environmental enrichment improves response strength, threshold, selectivity, and latency of auditory cortex neurons. J. Neurophysiol. 92 (2004) 73-82
30. Erwin R.J., Mawhinney-Hee M., Gur R.C., and Gur R.E. Midlatency auditory evoked responses in schizophrenia. Biol. Psychiatry 30 (1991) 430-442
31. Farmer J., Zhao X., van Praag H., Wodtke K., Gage F.H., and Christie B.R. Effects of voluntary exercise on synaptic plasticity and gene expression in the dentate gyrus of adult male Sprague-Dawley rats in vivo. Neuroscience 124 (2004) 71-79
32. Ferchmin P.A., and Bennett E.L. Direct contact with enriched environment is required to alter cerebral weights in rats. J. Comp. Physiol. Psychol. 88 (1975) 360-367
33. Ferriera G., Meurisse M., Gervais R., Ravel I.V., and Levy F. Extensive immunolesions of basal forebrain cholinergic system impair offspring recognition in sheep. Neuroscience 106 (2001) 103-116
34. Freedman R., Adler L.E., Bickford P., Byerley W., Coon H., Cullum C.M., Griffith J.M., Harris J.G., Leonard S., and Miller C. Schizophrenia and nicotinic receptors. Harv. Rev. Psychiatry 2 (1994) 179-192
35. Frenkel M.Y., Sawtell N.B., Diogo A.C., Yoon B., Neve R.L., and Bear M.F. Instructive effect of visual experience in mouse visual cortex. Neuron 51 (2006) 339-349
36. Galani R., Jeltsch H., Lehmann O., Bertrand F., and Cassel J.C. Effects of 192 IgG-saporin on acetylcholinesterase histochemistry in male and female rats. Brain Res. Bull. 58 (2002) 179-186
37. Geyer M.A., Wilkinson L.S., Humby T., and Robbins T.W. Isolation rearing of rats produces a deficit in prepulse inhibition of acoustic startle similar to that in schizophrenia. Biol. Psychiatry 34 (1993) 361-372
38. Gil-Bea E.J., Garcia-Alloza M., Dominguez J., Marcos B., and Ramirez M.J. Evaluation of cholinergic markers in Alzheimer's disease and in a model of cholinergic deficit. Neurosci. Lett. 375 (2005) 37-41
39. Gilley P.M., Sharma A., Dorman M., Finley C.C., Panch A.S., and Martin K. Minimization of cochlear implant stimulus artifact in cortical auditory evoked potentials. Clin. Neurophysiol. 117 (2006) 1772-1778
40. Gordon N.S., Burke S., Akil H., Watson S.J., and Panksepp J. Socially-induced brain 'fertilization': play promotes brain derived neurotrophic factor transcription in the amygdala and dorsolateral frontal cortex in juvenile rats. Neurosci. Lett. 341 (2003) 17-20
41. Greenough W.T., Volkmar F.R., and Juraska J.M. Effects of rearing complexity on dendritic branching in frontolateral and temporal cortex of the rat. Exp. Neurol. 41 (1973) 371-378
42. Gu Q. Neuromodulatory transmitter systems in the cortex and their role in cortical plasticity. Neuroscience 111 (2002) 815-835
43. Gu Q., and Singer W. Effects of intracortical infusion of anticholinergic drugs on neuronal plasticity in kitten striate cortex. Eur. J. Neurosci. 5 (1993) 475-485
44. Hasselmo M.E. Neuromodulation and cortical function: modeling the physiological basis of behavior. Behav. Brain Res. 67 (1995) 1-27
45. Hayes E.A., Warrier C.M., Nicol T.G., Zecker S.G., and Kraus N. Neural plasticity following auditory training in children with learning problems. Clin. Neurophysiol. 114 (2003) 673-684
46. Heckers S., Ohtake T., Wiley R.G., Lappi D.A., Geula C., and Mesulam M.M. Complete and selective cholinergic denervation of rat neocortex and hippocampus but not amygdala by an immunotoxin against the p75 NGF receptor. J. Neurosci. 14 (1994) 1271-1289
47. Ickes B.R., Pham T.M., Sanders L.A., Albeck D.S., Mohammed A.H., and Granholm A.C. Long-term environmental enrichment leads to regional increases in neurotrophin levels in rat brain. Exp. Neurol. 164 (2000) 45-52
48. Ivliev D.A. The effects of atropine microinjections into the motor cortex of rats on the development of a motor habit. Neurosci. Behav. Physiol. 29 (1999) 371-375
49. Jessen F., Kucharski C., Fries T., Papassotiropoulos A., Hoenig K., Maier W., and Heun R. Sensory gating deficit expressed by a disturbed suppression of the P50 event-related potential in patients with Alzheimer's disease. Am. J. Psychiatry 158 (2001) 1319-1321
50. Johansson B.B. Environmental influence on recovery after brain lesions-experimental and clinical data. J. Rehabil. Med. 41 (2003) 11-16
51. Juliano S.L., Ma W., and Eslin D. Cholinergic depletion prevents expansion of topographic maps in somatosensory cortex. Proc. Natl. Acad. Sci. U. S. A. 88 (1991) 780-784
52. Juliano S.L., Ma W., Bear M.F., and Eslin D. Cholinergic manipulation alters stimulus-evoked metabolic activity in cat somatosensory cortex. J. Comp. Neurol. 297 (1990) 106-120
53. Kamke M.R., Brown M., and Irvine D.R. Origin and immunolesioning of cholinergic basal forebrain innervation of cat primary auditory cortex. Hear. Res. 206 (2005) 89-106
54. Karnovsky M.J., and Roots L. A "direct-coloring" thiocholine method for cholinesterases. J. Histochem. Cytochem. 12 (1964) 219-221
55. Katz H.B., and Davies C.A. Effects of differential environments on the cerebral anatomy of rats as a function of previous and subsequent housing conditions. Exp. Neurol. 83 (1984) 274-287
56. Kilgard M.P., and Merzenich M.M. Cortical map reorganization enabled by nucleus basalis activity. Science 279 (1998) 1714-1718
57. Kilgard M.P., and Merzenich M.M. Plasticity of temporal information processing in the primary auditory cortex. Nat. Neurosci. 1 (1998) 727-731
58. Kiss J., McGovern J., and Patel A.J. Immunohistochemical localization of cells containing nerve growth factor receptors in the different regions of the adult rat forebrain. Neuroscience 27 (1988) 731-748
59. Kudoh M., Seki K., and Shibuki K. Sound sequence discrimination learning is dependent on cholinergic inputs to the rat auditory cortex. Neurosci. Res. 50 (2004) 113-123
60. Kuhl P.K., Tsao F.M., and Liu H.M. Foreign-language experience in infancy: effects of short-term exposure and social interaction on phonetic learning. Proc. Natl. Acad. Sci. U. S. A. 100 15 (2003) 9096-9101
61. Kuriki S., Kanda S., and Hirata Y. Effects of musical experience on different components of MEG responses elicited by sequential piano-tones and chords. J. Neurosci. 26 (2006) 4046-4053
62. Lewis E.M., Barnett Jr. J.F., Freshwater L., Hoberman A.M., and Christian M.S. Sexual maturation data for Crl Sprague-Dawley rats: criteria and confounding factors. Drug Chem. Toxicol. 25 (2002) 437-458
63. Merzenich M.M., Jenkins W.M., Johnston P., Schreiner C., Miller S.L., and Tallal P. Temporal processing deficits of language-learning impaired children ameliorated by training. Science 271 (1996) 77-81
64. Merzenich M.M., Saunders G., Jenkins W.M., Miller S., Peterson B.E., and Tallal P. Pervasive developmental disorders: listening training and language abilities. In: Broman S.H., and Fletcher J.M. (Eds). The Changing Nervous System: Neurobehavioral Consequences of Early Brain Disorders (1999), Oxford University Press, Oxford 365-385
65. Metherate R., and Weinberger N.M. Acetylcholine produces stimulus-specific receptive field alterations in cat auditory cortex. Brain Res. 480 (1989) 372-377
66. Metherate R., Tremblay N., and Dykes R.W. Acetylcholine permits long-term enhancement of neuronal responsiveness in cat primary somatosensory cortex. Neuroscience 22 (1987) 75-81
67. Moncek F., Duncko R., Johansson B.B., and Jezova D. Effects of environmental enrichment on stress related systems in rats. J. Neuroendocrinol. 16 (2004) 423-431
68. Motooka Y., Kondoh T., Nomura T., Tamaki N., Tozaki H., Kanno T., and Nishizaki T. Selective cholinergic denervation inhibits expression of long-term potentiation in the adult but not infant rat hippocampus. Dev. Brain Res. 129 (2001) 119-123
69. Nagarajan S.S., Wang X., Merzenich M.M., Schreiner C.E., Johnston P., Jenkins W.M., Miller S., and Tallal P. Speech modifications algorithms used for training language learning-impaired children. IEEE Trans. Rehabil. Eng. 6 (1998) 257-268
70. Nagarajan S.S., Mahncke H., Salz T., Tallal P., Roberts T., and Merzenich M.M. Cortical auditory signal processing in poor readers. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 6483-6488
71. Naka F., Shiga T., Yaguchi M., and Okado N. An enriched environment increases noradrenaline concentration in the mouse brain. Brain Res. 924 (2002) 124-126
72. Neeper S.A., Gomez-Pinilla F., Choi J., and Cotman C.W. Physical activity increases mRNA for brain-derived neurotrophic factor and nerve growth factor in rat brain. Brain Res. 726 (1996) 49-56
73. Nichols J., Jakkamsetti V., Dinh L., Kilgard M.P., and Atzori M. Environmental enrichment selectively increases glutamatergic responses in layer II/III of the auditory cortex of the rat. Neuroscience 145 (2007) 832-840
74. O'Shea L., Saari M., Pappas B.A., Ings R., and Stange K. Neonatal 6-hydroxydopamine attenuates the neural and behavioral effects of enriched rearing in the rat. Eur. J. Pharmacol. 92 (1983) 43-47
75. Paban V., Chambon C., Jaffard M., and Alescio-Lautier B. Behavioral effects of basal forebrain cholinergic lesions in young adult and aging rats. Behav. Neurosci. 119 (2005) 933-945
76. Park G.A., Pappas B.A., Murtha S.M., and Ally A. Enriched environment primes forebrain choline acetyltransferase activity to respond to learning experience. Neurosci. Lett. 143 (1992) 259-262
77. Paxinos G., and Watson C. The Rat Brain in Stereotaxic Coordinates (1998), Academic Press, San Diego, CA
78. Percaccio C.R., Engineer N.D., Pruette A.L., Pandya P.K., Moucha R., Rathbun D.L., and Kilgard M.P. Environmental enrichment increases paired-pulse depression in rat auditory cortex. J. Neurophysiol. 94 (2005) 3590-3600
79. Perry E.K., Tomlinson B.E., Blessed G., Bergmann K., Gibson P.H., and Perry R.H. Correlation of cholinergic abnormalities with senile plaques and mental test scores in senile dementia. Br. Med. J. 2 (1978) 1457-1459
80. Perry E.K., Lee M.L., Martin-Ruiz C.M., Court J.A., Volsen S.G., Merrit J., Folly E., Iversen P.E., Bauman M.L., Perry R.H., and Wenk G.L. Cholinergic activity in autism: abnormalities in the cerebral cortex and basal forebrain. Am. J. Psychiatry 158 (2001) 1058-1066
81. Perry W., Minassian A., Lopez B., Maron L., and Lincoln A. Sensorimotor gating deficits in adults with autism. Biol. Psychiatry 61 (2006) 481-486
82. Ponton C.W., Vasama J.P., Tremblay K., Khosla D., Kwong B., and Don M. Plasticity in the adult human central auditory system: evidence from late-onset profound unilateral deafness. Hear. Res. 154 (2001) 32-44
83. Por S.B., Bennett E.L., and Bondy S.C. Environmental enrichment and neurotransmitter receptors. Behav. Neural Biol. 34 (1982) 132-140
84. Preece M.A., Dalley J.W., Theobald D.E., Robbins T.W., and Reynolds G.P. Region specific changes in forebrain 5-hydroxytryptamine1A and 5-hydroxytryptamine2A receptors in isolation-reared rats: an in vitro autoradiography study. Neuroscience 123 (2004) 725-732
85. Recanzone G.H., Schreiner C.E., and Merzenich M.M. Plasticity in the frequency representation of primary auditory cortex following discrimination training in adult owl monkeys. J. Neurosci. 13 (1993) 87-103
86. Renner M.J., and Rosenzweig M.R. Social interactions among rats housed in grouped and enriched conditions. Dev. Psychobiol. 19 (1986) 303-313
87. Richardson R.T., and DeLong M.R. Electrophysiological studies of the functions of the nucleus basalis in primates. Adv. Exp. Med. Biol. 295 (1991) 233-252
88. Risedal A., Mattsson B., Dahlqvist P., Nordborg C., Olsson T., and Johansson B.B. Environmental influences on functional outcome after a cortical infarct in the rat. Brain Res. Bull. 58 (2002) 315-321
89. Rosenzweig M.R., Bennett E.L., and Diamond M.C. Cerebral effects of differential experience in hypophysectomized rats. J. Comp. Physiol. Psychol. 79 (1972) 56-66
90. Rosenzweig M.R., Bennett E.L., Hebert M., and Morimoto H. Social grouping cannot account for cerebral effects of enriched environments. Brain Res. 153 (1978) 563-576
91. Sato H., Hata Y., Hagiharak K., and Tsumoto T. Effect of cholinergic depletion on neuron activity in the cat visual cortex. J. Neurophysiol. 58 (1987) 781-794
92. Seitz A.R., and Dinse H.R. A common framework for perceptual learning. Curr. Opin. Neurobiol. 17 (2007) 148-153
93. Sharma A., Tobey E., Dorman M., Bharadwaj S., Martin K., Gilley P., and Kunkel F. Central auditory maturation and babbling development in infants with cochlear implants. Arch. Otolaryngol. Head Neck Surg. 130 (2004) 511-516
94. Stranahan A.M., Khalil D., and Gould E. Social isolation delays the positive effects of running on adult neurogenesis. Nat. Neurosci. 9 (2006) 526-533
95. Stummer W., Weber K., Tranmer B., Baethmann A., and Kempski O. Reduced mortality and brain damage after locomotor activity in gerbil forebrain ischemia. Stroke 25 (1994) 1862-1869
96. Swain R.A., Harris A.B., Wiener E.C., Dutka M.V., Morris H.D., Theien B.E., Konda S., Engberg K., Lauterbur P.C., and Greenough W.T. Prolonged exercise induces angiogenesis and increases cerebral blood volume in primary motor cortex of the rat. Neuroscience 117 (2003) 1037-1046
97. Tallal P., Miller S.L., Bedi G., Byma G., Wang X., Nagarajan S.S., Schreiner C., Jenkins W.M., and Merzenich M.M. Language comprehension in language-learning impaired children improved with acoustically modified speech. Science 271 (1996) 81-84
98. Tallal P., Merzenich M.M., Miller S., and Jenkins W. Language learning impairments: integrating basic science, technology, and remediation. Exp. Brain Res. 123 (1998) 210-219
99. Tremblay K., Kraus N., McGee T., Ponton C., and Otis B. Central auditory plasticity: changes in the N1-P2 complex after speech-sound training. Ear Hear. 22 (2001) 79-90
100. Turner A.M., and Greenough W.T. Differential rearing effects on rat visual cortex synapses. I. Synaptic and neuronal density and synapses per neuron. Brain Res. 329 (1985) 195-203
101. van Praag H., Kempermann G., and Gage F.H. Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat. Neurosci. 2 (1999) 266-270
102. van Praag H., Kempermann G., and Gage F.H. Neural consequences of environmental enrichment. Nat. Rev., Neurosci. 1 (2000) 191-198
103. Verdier D., and Dykes R.W. Long-term cholinergic enhancement of evoked potentials in rat hindlimb somatosensory cortex displays characteristics of long-term potentiation. Exp. Brain Res. 137 (2001) 71-82
104. Waite J.J., and Chen A.D. Differential changes in rat cholinergic parameters subsequent to immunotoxic lesion of the basal forebrain nuclei. Brain Res. 918 (2001) 113-120
105. Waite J.J., Chen A.D., Wardlow M.L., Wiley R.G., Lappi D.A., and Thal L.J. 192 immunoglobulin G-saporin produces graded behavioral and biochemical changes accompanying the loss of cholinergic neurons of the basal forebrain and cerebellar Purkinje cells. Neuroscience 65 (1995) 463-476
106. Waite J.J., Wardlow M.L., Chen A.C., Lappi D.A., Wiley R.G., and Thal L.J. Time course of cholinergic and monoaminergic changes in rat brain after immunolesioning with 192 IgG-saporin. Neurosci. Lett. 169 (1994) 154-158
107. Warrier C.M., Johnson K.L., Hayes E.A., Nicol T., and Kraus N. Learning impaired children exhibit timing deficits and training-related improvements in auditory cortical responses to speech in noise. Exp. Brain Res. 157 (2004) 431-441
108. Walsh T.J., Kelly R.M., Dougherty K.D., Stackman R.W., Wiley R.G., and Kutscher C.L. Behavioral and neurobiological alterations induced by the immunotoxin 192-IgG-saporin: cholinergic and non-cholinergic effects following i.c.v. injection. Brain Res. 702 (1995) 233-245
109. Webster H.H., Hanisch U.K., Dykes R.W., and Biesold D. Basal forebrain lesions with or without reserpine injection inhibit cortical reorganization in rat hindpaw primary somatosensory cortex following sciatic nerve section. Somatosens Mot. Res. 8 (1991) 327-346
110. Wenk H., Bigl V., and Meyer U. Cholinergic projections from magnocellular nuclei of the basal forebrain to cortical areas in rats. Brain Res. 2 (1980) 295-316
111. Wenk G.L. Rett syndrome: neurobiological changes underlying specific symptoms. Prog. Neurobiol. 51 (1997) 383-391
112. Wible B., Nicol T., and Kraus N. Abnormal neural encoding of repeated speech stimuli in noise in children with learning problems. Clin. Neurophysiol. 113 (2002) 485-494
113. Wiley R.G., Berbos T.G., Deckwerth T.L., Johnson Jr. E.M., and Lappi D.A. Destruction of the cholinergic basal forebrain using immunotoxin to rat NGF receptor: modeling the cholinergic degeneration of Alzheimer's disease. J. Neurol. Sci. 128 (1995) 157-166
114. Wiley R.G., Oeltmann T.N., and Lappi D.A. Immunolesioning: selective destruction of neurons using immunotoxin to rat NGF receptor. Brain Res. 562 (1991) 149-153
115. Wrenn C.C., and Wiley R.G. The behavioral functions of the cholinergic basal forebrain: lessons from 192 IgG-saporin. Int. J. Dev. Neurosci. 16 7 (1998) 595-602