The role of cortical inhibition in the pathophysiology and treatment of schizophrenia

Brain Research Reviews

Volumn 56, Issue 2, 2007, Pages 427-442

  Daskalakis, Zafiris J ^a   Fitzgerald, Paul B ^b   Christensen, Bruce K ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b Monash University   (Australia)

Author keywords

Antipsychotic; GABA; Inhibition cortex; Interneuron; Schizophrenia; Transcranial magnetic stimulation

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID RECEPTOR STIMULATING AGENT; BACLOFEN; BENZODIAZEPINE DERIVATIVE; BRETAZENIL; BUNGAROTOXIN RECEPTOR; CLOZAPINE; DOPAMINE 2 RECEPTOR BLOCKING AGENT; FLUPHENAZINE; GLUTAMIC ACID; HALOPERIDOL; NEUROLEPTIC AGENT; OLANZAPINE;

BRAIN CORTEX; BRAIN CORTEX INHIBITION; DISEASE MODEL; DRUG MECHANISM; GABAERGIC TRANSMISSION; GENETIC POLYMORPHISM; HUMAN; INTERNEURON; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REVIEW; SCHIZOPHRENIA; SYMPTOM; TRANSCRANIAL MAGNETIC STIMULATION;

ANIMALS; CEREBRAL CORTEX; GAMMA-AMINOBUTYRIC ACID; GLUTAMIC ACID; HUMANS; INTERNEURONS; SCHIZOPHRENIA;

EID: 36549005181     PISSN: 01650173     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainresrev.2007.09.006     Document Type: Review

References (149)

1. Adler L.E., Pachtman E., Franks R.D., Pecevich M., Waldo M.C., and Freedman R. Neurophysiological evidence for a defect in neuronal mechanisms involved in sensory gating in schizophrenia. Biol. Psychiatry 17 (1982) 639-654
2. Adler L.E., Gerhardt G.A., Franks R., Baker N., Nagamoto H., Drebing C., and Freedman R. Sensory physiology and catecholamines in schizophrenia and mania. Psychiatry Res. 31 (1990) 297-309
3. Adler L.E., Hoffer L.J., Griffith J., Waldo M.C., and Freedman R. Normalization by nicotine of deficient auditory sensory gating in the relatives of schizophrenics. Biol. Psychiatry 32 (1992) 607-616
4. Adler L.E., Hoffer L.D., Wiser A., and Freedman R. Normalization of auditory physiology by cigarette smoking in schizophrenic patients. Am. J. Psychiatry 150 (1993) 1856-1861
5. Adler L.E., Olincy A., Cawthra E.M., McRae K.A., Harris J.G., Nagamoto H.T., Waldo M.C., Hall M.H., Bowles A., Woodward L., Ross R.G., and Freedman R. Varied effects of atypical neuroleptics on P50 auditory gating in schizophrenia patients. Am. J. Psychiatry 161 (2004) 1822-1828
6. Akbarian S., Kim J.J., Potkin S.G., Hagman J.O., Tafazzoli A., Bunney Jr. W.E., and Jones E.G. Gene expression for glutamic acid decarboxylase is reduced without loss of neurons in prefrontal cortex of schizophrenics [see comments]. Arch. Gen. Psychiatry 52 (1995) 258-266 (discussion 267-78)
7. Arnold S.E., Franz B.R., Gur R.C., Gur R.E., Shapiro R.M., Moberg P.J., and Trojanowski J.Q. Smaller neuron size in schizophrenia in hippocampal subfields that mediate cortical-hippocampal interactions. Am. J. Psychiatry 152 (1995) 738-748
8. Baddeley A.D. Working Memory (1986), Oxford University Press, Oxford
9. Bajbouj M., Lang U.E., Niehaus L., Hellen F.E., Heuser I., and Neu P. Effects of right unilateral electroconvulsive therapy on motor cortical excitability in depressive patients. J. Psychiatr. Res. 40 (2006) 322-327
10. Baron R.M., and Kenny D.A. The moderator-mediator variable distinction in social psychological research: conceptual, strategic, and statistical considerations. J. Pers. Soc. Psychol. 51 (1986) 1173-1182
11. Basar-Eroglu C., Struber D., Schurmann M., Stadler M., and Basar E. Gamma-band responses in the brain: a short review of psychophysiological correlates and functional significance. Int. J. Psychophysiol. 24 (1996) 101-112
12. Benes F.M. The role of stress and dopamine-GABA interactions in the vulnerability for schizophrenia. J. Psychiatr. Res. 31 (1997) 257-275
13. Benes F.M. Model generation and testing to probe neural circuitry in the cingulate cortex of postmortem schizophrenic brain. Schizophr. Bull. 24 (1998) 219-230
14. Benes F.M., and Berretta S. GABAergic interneurons: implications for understanding schizophrenia and bipolar disorder. Neuropsychopharmacology 25 (2001) 1-27
15. Benes F.M., and Lange N. Two-dimensional versus three-dimensional cell counting: a practical perspective. Trends Neurosci. 24 (2001) 11-17
16. Benes F.M., McSparren J., Bird E.D., SanGiovanni J.P., and Vincent S.L. Deficits in small interneurons in prefrontal and cingulate cortices of schizophrenic and schizoaffective patients. Arch. Gen. Psychiatry 48 (1991) 996-1001
17. Benes F.M., Todtenkopf M.S., and Taylor J.B. Differential distribution of tyrosine hydroxylase fibers on small and large neurons in layer II of anterior cingulate cortex of schizophrenic brain. Synapse 25 (1997) 80-92
18. Benes F.M., Todtenkopf M.S., and Taylor J.B. Differential distribution of tyrosine hydroxylase fibers on small and large neurons in layer II of anterior cingulate cortex of schizophrenic brain. Synapse 25 (1997) 80-92
19. Bickford-Wimer P.C., Nagamoto H., Johnson R., Adler L.E., Egan M., Rose G.M., and Freedman R. Auditory sensory gating in hippocampal neurons: a model system in the rat. Biol. Psychiatry 27 (1990) 183-192
20. Boutros N.N., Overall J., and Zouridakis G. Test-retest reliability of the P50 mid-latency auditory evoked response. Psychiatry Res. 39 (1991) 181-192
21. Butefisch C.M., Davis B.C., Wise S.P., Sawaki L., Kopylev L., Classen J., and Cohen L.G. Mechanisms of use-dependent plasticity in the human motor cortex. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 3661-3665
22. Cabib S., and Puglisi-Allegra S. Stress, depression and the mesolimbic dopamine system. Psychopharmacology (Berl.) 128 (1996) 331-342
23. Cantello R., Gianelli M., Civardi C., and Mutani R. Magnetic brain stimulation: the silent period after the motor evoked potential. Neurology 42 (1992) 1951-1959
24. Carpenter Jr. W.T., Buchanan R.W., Kirkpatrick B., and Breier A.F. Diazepam treatment of early signs of exacerbation in schizophrenia. Am. J. Psychiatry 156 (1999) 299-303
25. Chen R., Classen J., Gerloff C., Celnik P., Wassermann E.M., Hallett M., and Cohen L.G. Depression of motor cortex excitability by low-frequency transcranial magnetic stimulation. Neurology 48 (1997) 1398-1403
26. Chen R., Corwell B., Yaseen Z., Hallett M., and Cohen L.G. Mechanisms of cortical reorganization in lower-limb amputees. J. Neurosci. 18 (1998) 3443-3450
27. Chini B., Raimond E., Elgoyhen A.B., Moralli D., Balzaretti M., and Heinemann S. Molecular cloning and chromosomal localization of the human alpha 7-nicotinic receptor subunit gene (CHRNA7). Genomics 19 (1994) 379-381
28. Cho R.Y., Konecky R.O., and Carter C.S. Impairments in frontal cortical gamma synchrony and cognitive control in schizophrenia. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 19878-19883
29. Chouinard G., Annable L., Turnier L., Holobow N., and Szkrumelak N. A double-blind randomized clinical trial of rapid tranquilization with I.M. clonazepam and I.M. haloperidol in agitated psychotic patients with manic symptoms. Can. J. Psychiatry 38 Suppl 4 (1993) S114-S121
30. Cohen J. Statistical Power Analysis for the Behavioral Sciences. 2nd ed. (1988), Lawrence Erlbaum Associates, Hillsdale, New Jersey
31. Costa E., Davis J., Grayson D.R., Guidotti A., Pappas G.D., and Pesold C. Dendritic spine hypoplasticity and downregulation of reelin and GABAergic tone in schizophrenia vulnerability. Neurobiol. Dis. 8 (2001) 723-742
32. Court J., Spurden D., Lloyd S., McKeith I., Ballard C., Cairns N., Kerwin R., Perry R., and Perry E. Neuronal nicotinic receptors in dementia with Lewy bodies and schizophrenia: alpha-bungarotoxin and nicotine binding in the thalamus. J. Neurochem. 73 (1999) 1590-1597
33. Daskalakis Z.J., Christensen B.K., Chen R., Fitzgerald P.B., Zipursky R.B., and Kapur S. Evidence for impaired cortical inhibition in schizophrenia using transcranial magnetic stimulation. Arch. Gen. Psychiatry 59 (2002) 347-354
34. Daskalakis Z.J., Christensen B.K., Fitzgerald P.B., Roshan L., and Chen R. The mechanisms of interhemispheric inhibition in the human motor cortex. J. Physiol. 543 (2002) 317-326
35. Daskalakis Z.J., Moller B., Christensen B.K., Fitzgerald P.B., Gunraj C., and Chen R. The effects of repetitive transcranial magnetic stimulation on cortical inhibition in healthy human subjects. Exp. Brain Res. 174 (2006) 403-412
36. Daskalakis, Z.J., Chrisensen, B.K., Fitzgerald, P.B., Möller, B.M., Fountain, S.I., Chen, R., in press. Increased cortical inhibition in persons with schizophrenia treated with clozapine. J. of Psychopharmacol.
37. De Luca V., Voineskos S., Wong G., and Kennedy J.L. Genetic interaction between alpha4 and beta2 subunits of high affinity nicotinic receptor: analysis in schizophrenia. Exp. Brain Res. 174 (2006) 292-296
38. Deco G., and Rolls E.T. Attention and working memory: a dynamical model of neuronal activity in the prefrontal cortex. Eur. J. Neurosci. 18 (2003) 2374-2390
39. DeFelipe J., and Farinas I. The pyramidal neuron of the cerebral cortex: morphological and chemical characteristics of the synaptic inputs. Prog. Neurobiol. 39 (1992) 563-607
40. DeFelipe J., Conley M., and Jones E.G. Long-range focal collateralization of axons arising from corticocortical cells in monkey sensory-motor cortex. J. Neurosci. 6 (1986) 3749-3766
41. Delawalla Z., Barch D.M., Fisher Eastep J.L., Thomason E.S., Hanewinkel M.J., Thompson P.A., and Csernansky J.G. Factors mediating cognitive deficits and psychopathology among siblings of individuals with schizophrenia. Schizophr. Bull. 32 (2006) 525-537
42. Delini-Stula A., and Berdah-Tordjman D. Antipsychotic effects of bretazenil, a partial benzodiazepine agonist in acute schizophrenia-a study group report. J. Psychiatr. Res. 30 (1996) 239-250
43. Farber N.B., Newcomer J.W., and Olney J.W. Glycine agonists: what can they teach us about schizophrenia? [comment]. Arch. Gen. Psychiatry. 56 (1999) 13-17
44. Farnbach-Pralong D., Bradbury R., Copolov D., and Dean B. Clozapine and olanzapine treatment decreases rat cortical and limbic GABA(A) receptors. Eur. J. Pharmacol. 349 (1998) R7-R8
45. Fitzgerald P.B., Brown T.L., Daskalakis Z.J., deCastella A., and Kulkarni J. A study of transcallosal inhibition in schizophrenia using transcranial magnetic stimulation. Schizophr. Res. 56 (2002) 199-209
46. Fitzgerald P.B., Brown T.L., Daskalakis Z.J., and Kulkarni J. A transcranial magnetic stimulation study of inhibitory deficits in the motor cortex in patients with schizophrenia. Psychiatry Res. 114 (2002) 11-22
47. Fitzgerald P.B., Brown T.L., Marston N.A., Oxley T.J., de Castella A., Daskalakis Z.J., and Kulkarni J. A transcranial magnetic stimulation study of abnormal cortical inhibition in schizophrenia. Psychiatry Res. 118 (2003) 197-207
48. Fitzgerald P.B., Benitez J., Daskalakis J.Z., Brown T.L., Marston N.A., de Castella A., and Kulkarni J. A double-blind sham-controlled trial of repetitive transcranial magnetic stimulation in the treatment of refractory auditory hallucinations. J. Clin. Psychopharmacol. 25 (2005) 358-362
49. Frantseva, M.V., Fitzgerald, P.B., Chen, R., Moller, B., Daigle, M., Daskalakis, Z.J., in press. Evidence for impaired long-term potentiation in schizophrenia and its relationship to motor skill leaning. Cerebral Cortex.
50. Freedman R., Adler L.E., Waldo M.C., Pachtman E., and Franks R.D. Neurophysiological evidence for a defect in inhibitory pathways in schizophrenia: comparison of medicated and drug-free patients. Biol. Psychiatry 18 (1983) 537-551
51. Freedman R., Waldo M., Bickford-Wimer P., and Nagamoto H. Elementary neuronal dysfunctions in schizophrenia. Schizophr. Res. 4 (1991) 233-243
52. Freedman R., Wetmore C., Stromberg I., Leonard S., and Olson L. Alpha-bungarotoxin binding to hippocampal interneurons: immunocytochemical characterization and effects on growth factor expression. J. Neurosci. 13 (1993) 1965-1975
53. Freedman R., Hall M., Adler L.E., and Leonard S. Evidence in postmortem brain tissue for decreased numbers of hippocampal nicotinic receptors in schizophrenia. Biol. Psychiatry 38 (1995) 22-33
54. Freedman R., Adler L.E., Myles-Worsley M., Nagamoto H.T., Miller C., Kisley M., McRae K., Cawthra E., and Waldo M. Inhibitory gating of an evoked response to repeated auditory stimuli in schizophrenic and normal subjects. Human recordings, computer simulation, and an animal model. Arch. Gen. Psychiatry 53 (1996) 1114-1121
55. Freedman R., Coon H., Myles-Worsley M., Orr-Urtreger A., Olincy A., Davis A., Polymeropoulos M., Holik J., Hopkins J., Hoff M., Rosenthal J., Waldo M.C., Reimherr F., Wender P., Yaw J., Young D.A., Breese C.R., Adams C., Patterson D., Adler L.E., Kruglyak L., Leonard S., and Byerley W. Linkage of a neurophysiological deficit in schizophrenia to a chromosome 15 locus. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 587-592
56. Freedman R., Adams C.E., Adler L.E., Bickford P.C., Gault J., Harris J.G., Nagamoto H.T., Olincy A., Ross R.G., Stevens K.E., Waldo M., and Leonard S. Inhibitory neurophysiological deficit as a phenotype for genetic investigation of schizophrenia. Am. J. Med. Genet. 97 (2000) 58-64
57. Freedman R., Leonard S., Gault J.M., Hopkins J., Cloninger C.R., Kaufmann C.A., Tsuang M.T., Farone S.V., Malaspina D., Svrakic D.M., Sanders A., and Gejman P. Linkage disequilibrium for schizophrenia at the chromosome 15q13-14 locus of the alpha7-nicotinic acetylcholine receptor subunit gene (CHRNA7). Am. J. Med. Genet. 105 (2001) 20-22
58. Gejman P.V., Sanders A.R., Badner J.A., Cao Q., and Zhang J. Linkage analysis of schizophrenia to chromosome 15. Am. J. Med. Genet. 105 (2001) 789-793
59. Geyer M.A., and Braff D.L. Startle habituation and sensorimotor gating in schizophrenia and related animal models. Schizophr. Bull. 13 (1987) 643-668
60. Gonzalez-Burgos G., Kroener S., Seamans J.K., Lewis D.A., and Barrionuevo G. Dopaminergic modulation of short-term synaptic plasticity in fast-spiking interneurons ofprimate dorsolateral prefrontal cortex. J. Neurophysiol. 94 (2005) 4168-4177
61. Gorelova N., Seamans J.K., and Yang C.R. Mechanisms of dopamine activation of fast-spiking interneurons that exert inhibition in rat prefrontal cortex. J. Neurophysiol. 88 (2002) 3150-3166
62. Greenberg B.D., Ziemann U., Cora-Locatelli G., Harmon A., Murphy D.L., Keel J.C., and Wassermann E.M. Altered cortical excitability in obsessive-compulsive disorder. Neurology 54 (2000) 142-147
63. Griffith J., Hoffer L.D., Adler L.E., Zerbe G.O., and Freedman R. Effects of sound intensity on a midlatency evoked response to repeated auditory stimuli in schizophrenic and normal subjects. Psychophysiology 32 (1995) 460-466
64. Guan Z.Z., Zhang X., Blennow K., and Nordberg A. Decreased protein level of nicotinic receptor alpha7 subunit in the frontal cortex from schizophrenic brain. NeuroReport 10 (1999) 1779-1782
65. Hebb D.O. The Organization of Behavior. A Neuropsychological Theory (1949), Wiley, New York
66. Hershman K.M., Freedman R., and Bickford P.C. GABAB antagonists diminish the inhibitory gating of auditory response in the rat hippocampus. Neurosci. Lett. 190 (1995) 133-136
67. Hess G., Aizenman C.D., and Donoghue J.P. Conditions for the induction of long-term potentiation in layer II/III horizontal connections of the rat motor cortex. J. Neurophysiol. 75 (1996) 1765-1778
68. Hoffman R.E., Boutros N.N., Berman R.M., Roessler E., Belger A., Krystal J.H., and Charney D.S. Transcranial magnetic stimulation of left temporoparietal cortex in three patients reporting hallucinated and "voices". Biol. Psychiatry 46 (1999) 130-132
69. Hoffman R.E., Hawkins K.A., Gueorguieva R., Boutros N.N., Rachid F., Carroll K., and Krystal J.H. Transcranial magnetic stimulation of left temporoparietal cortex and medication-resistant auditory hallucinations. Arch. Gen. Psychiatry 60 (2003) 49-56
70. Hong L.E., Wonodi I., Stine O.C., Mitchell B.D., and Thaker G.K. Evidence of missense mutations on the neuregulin 1 gene affecting function of prepulse inhibition. Biol. Psychiatry (2007)
71. Impagnatiello F., Guidotti A.R., Pesold C., Dwivedi Y., Caruncho H., Pisu M.G., Uzunov D.P., Smalheiser N.R., Davis J.M., Pandey G.N., Pappas G.D., Tueting P., Sharma R.P., and Costa E. A decrease of reelin expression as a putative vulnerability factor in schizophrenia. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 15718-15723
72. Ishikawa M., Mizukami K., Iwakiri M., and Asada T. Immunohistochemical and immunoblot analysis of gamma-aminobutyric acid B receptor in the prefrontal cortex of subjects with schizophrenia and bipolar disorder. Neurosci. Lett. 383 (2005) 272-277
73. Jacobs K.M., and Donoghue J.P. Reshaping the cortical motor map by unmasking latent intracortical connections. Science 251 (1991) 44-947
74. Jamra R.A., Becker T., Klopp N., Dahdouh F., Schulze T.G., Gross M., Deschner M., Schmal C., Illig T., Rietschel M., Propping P., Cichon S., Nothen M.M., and Schumacher J. No evidence for an association between variants at the gamma-amino-n-butyric acid type A receptor beta2 locus and schizophrenia. Psychiatr. Genet. 17 (2007) 43-45
75. Javitt D.C., Balla A., Nattini M., and Sershen H. Role of NMDA and GABAB receptors in cortical and subcortical dopaminergic regulation. In: Nemeroff C.B. (Ed). American College of Neuropsychopharmacology vol. 31 (2006), Nature Publishing Group, Hollywood, Florida S47
76. Jones E.G. GABAergic neurons and their role in cortical plasticity in primates. Cereb. Cortex 3 (1993) 361-372
77. Kaufmann C.A., Suarez B., Malaspina D., Pepple J., Svrakic D., Markel P.D., Meyer J., Zambuto C.T., Schmitt K., Matise T.C., Harkavy Friedman J.M., Hampe C., Lee H., Shore D., Wynne D., Faraone S.V., Tsuang M.T., and Cloninger C.R. NIMH genetics initiative millennium schizophrenia consortium: linkage analysis of African-American pedigrees. Am. J. Med. Genet. 81 (1998) 282-289
78. Krnjevic K. Role of GABA in cerebral cortex. Can. J. Physiol. Pharm. 75 (1997) 439-451
79. Kujirai T., Caramia M.D., Rothwell J.C., Day B.L., Thompson P.D., Ferbert A., Wroe S., Asselman P., and Marsden C.D. Corticocortical inhibition in human motor cortex. J. Physiol. (Lond.) 471 (1993) 501-519
80. Lee S.H., Kim W., Chung Y.C., Jung K.H., Bahk W.M., Jun T.Y., Kim K.S., George M.S., and Chae J.H. A double blind study showing that two weeks of daily repetitive TMS over the left or right temporoparietal cortex reduces symptoms in patients with schizophrenia who are having treatment-refractory auditory hallucinations. Neurosci. Lett. 376 (2005) 177-181
81. Leonard S., Gault J., Moore T., Hopkins J., Robinson M., Olincy A., Adler L.E., Cloninger C.R., Kaufmann C.A., Tsuang M.T., Faraone S.V., Malaspina D., Svrakic D.M., and Freedman R. Further investigation of a chromosome 15 locus in schizophrenia: analysis of affected sibpairs from the NIMH Genetics Initiative. Am. J. Med. Genet. 81 (1998) 308-312
82. Leonard S., Gault J., Hopkins J., Logel J., Vianzon R., Short M., Drebing C., Berger R., Venn D., Sirota P., Zerbe G., Olincy A., Ross R.G., Adler L.E., and Freedman R. Association of promoter variants in the alpha7 nicotinic acetylcholine receptor subunit gene with an inhibitory deficit found in schizophrenia. Arch. Gen. Psychiatry 59 (2002) 1085-1096
83. Levinson A.J., Young L.T., Fitzgerald P.B., and Daskalakis Z.J. Cortical inhibitory dysfunction in bipolar disorder: a study using transcranial magnetic stimulation. J. Clin. Psychopharmacol. 27 (2007) 493-497
84. Lewis D.A., Hashimoto T., and Volk D.W. Cortical inhibitory neurons and schizophrenia. Nat. Rev., Neurosci. 6 (2005) 312-324
85. Lieberman J.A., Stroup T.S., McEvoy J.P., Swartz M.S., Rosenheck R.A., Perkins D.O., Keefe R.S., Davis S.M., Davis C.E., Lebowitz B.D., Severe J., and Hsiao J.K. Effectiveness of antipsychotic drugs in patients with chronic schizophrenia. N. Engl. J. Med. 353 (2005) 1209-1223
86. Light G.A., Geyer M.A., Clementz B.A., Cadenhead K.S., and Braff D.L. Normal P50 suppression in schizophrenia patients treated with atypical antipsychotic medications. Am. J. Psychiatry 157 (2000) 767-771
87. Lin H.F., Liu Y.L., Liu C.M., Hung S.I., Hwu H.G., and Chen W.J. Neuregulin 1 gene and variations in perceptual aberration of schizotypal personality in adolescents. Psychol. Med. 35 (2005) 1589-1598
88. Liu C.M., Hwu H.G., Lin M.W., Ou-Yang W.C., Lee S.F., Fann C.S., Wong S.H., and Hsieh S.H. Suggestive evidence for linkage of schizophrenia to markers at chromosome 15q13-14 in Taiwanese families. Am. J. Med. Genet. 105 (2001) 658-661
89. Lo W.S., Lau C.F., Xuan Z., Chan C.F., Feng G.Y., He L., Cao Z.C., Liu H., Luan Q.M., and Xue H. Association of SNPs and haplotypes in GABAA receptor beta2 gene with schizophrenia. Mol. Psychiatry 9 (2004) 603-608
90. Lu B.Y., Edgar J.C., Jones A.P., Smith A.K., Huang M.X., Miller G.A., and Canive J.M. Improved test-retest reliability of 50-ms paired-click auditory gating using magnetoencephalography source modeling. Psychophysiology 44 (2007) 86-90
91. Luntz-Leybman V., Bickford P.C., and Freedman R. Cholinergic gating of response to auditory stimuli in rat hippocampus. Brain Res. 587 (1992) 130-136
92. McEvoy J.P., Lieberman J.A., Stroup T.S., Davis S.M., Meltzer H.Y., Rosenheck R.A., Swartz M.S., Perkins D.O., Keefe R.S., Davis C.E., Severe J., and Hsiao J.K. Effectiveness of clozapine versus olanzapine, quetiapine, and risperidone in patients with chronic schizophrenia who did not respond to prior atypical antipsychotic treatment. Am. J. Psychiatry 163 (2006) 600-610
93. Miller C.L., and Freedman R. The activity of hippocampal interneurons and pyramidal cells during the response of the hippocampus to repeated auditory stimuli. Neuroscience 69 (1995) 371-381
94. Moller B., Light G.A.., Fitzgerald P.B., Snyder J.S., Chen R., and Daskalakis Z.J. Relationship between P50 suppression and the cortical silent period. Neuroreport 18 (2007) 1503-1506
95. Nagamoto H.T., Adler L.E., Hea R.A., Griffith J.M., McRae K.A., and Freedman R. Gating of auditory P50 in schizophrenics: unique effects of clozapine. Biol. Psychiatry 40 (1996) 181-188
96. Nakamura H., Kitagawa H., Kawaguchi Y., and Tsuji H. Intracortical facilitation and inhibition after transcranial magnetic stimulation in conscious humans. J. Physiol. 498 (1997) 817-823
97. Norton N., Moskvina V., Morris D.W., Bray N.J., Zammit S., Williams N.M., Williams H.J., Preece A.C., Dwyer S., Wilkinson J.C., Spurlock G., Kirov G., Buckland P., Waddington J.L., Gill M., Corvin A.P., Owen M.J., and O'Donovan M.C. Evidence that interaction between neuregulin 1 and its receptor erbB4 increases susceptibility to schizophrenia. Am. J. Med. Genet., B, Neuropsychiatr. Genet. 141 (2006) 96-101
98. Olincy A., and Martin L. Diminished suppression of the P50 auditory evoked potential in bipolar disorder subjects with a history of psychosis. Am. J. Psychiatry 162 (2005) 43-49
99. Olney J.W., and Farber N.B. Glutamate receptor dysfunction and schizophrenia [see comments]. Arch. Gen. Psychiatry 52 (1995) 998-1007
100. Oxley T., Fitzgerald P.B., Brown T.L., de Castella A., Daskalakis Z.J., and Kulkarni J. Repetitive transcranial magnetic stimulation reveals abnormal plastic response to premotor cortex stimulation in schizophrenia. Biol. Psychiatry 56 (2004) 628-633
101. Palva J.M., Palva S., and Kaila K. Phase synchrony among neuronal oscillations in the human cortex. J. Neurosci. 25 (2005) 3962-3972
102. Perry W., and Braff D.L. Information-processing deficits and thought disorder in schizophrenia. Am. J. Psychiatry 151 (1994) 363-367
103. Pesold C., Impagnatiello F., Pisu M.G., Uzunov D.P., Costa E., Guidotti A., and Caruncho H.J. Reelin is preferentially expressed in neurons synthesizing gamma-aminobutyric acid in cortex and hippocampus of adult rats. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 3221-3226
104. Pesold C., Liu W.S., Guidotti A., Costa E., and Caruncho H.J. Cortical bitufted, horizontal, and Martinotti cells preferentially express and secrete reelin into perineuronal nets, nonsynaptically modulating gene expression. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 3217-3222
105. Petryshen T.L., Middleton F.A., Tahl A.R., Rockwell G.N., Purcell S., Aldinger K.A., Kirby A., Morley C.P., McGann L., Gentile K.L., Waggoner S.G., Medeiros H.M., Carvalho C., Macedo A., Albus M., Maier W., Trixler M., Eichhammer P., Schwab S.G., Wildenauer D.B., Azevedo M.H., Pato M.T., Pato C.N., Daly M.J., and Sklar P. Genetic investigation of chromosome 5q GABAA receptor subunit genes in schizophrenia. Mol. Psychiatry 10 (2005) 1074-1088 (1057)
106. 3H]GABA in the rat prefrontal cortex. Neuroscience 43 (1991) 323-329
107. Riley B.P., Makoff A., Mogudi-Carter M., Jenkins T., Williamson R., Collier D., and Murray R. Haplotype transmission disequilibrium and evidence for linkage of the CHRNA7 gene region to schizophrenia in Southern African Bantu families. Am. J. Med. Genet. 96 (2000) 196-201
108. Roick H., von Giesen H.J., and Benecke R. On the origin of the postexcitatory inhibition seen after transcranial magnetic brain stimulation in awake human subjects. Exp. Brain Res. 94 (1993) 489-498
109. Romeo S., Gilio F., Pedace F., Ozkaynak S., Inghilleri M., Manfredi M., and Berardelli A. Changes in the cortical silent period after repetitive magnetic stimulation of cortical motor areas. Exp. Brain Res. 135 (2000) 504-510
110. Rosenthal D. Genetic Theory and Abnormal Behaviour (1970), McGraw-Hill, New York
111. Sackeim H.A., Luber B., Katzman G.P., Moeller J.R., Prudic J., Devanand D.P., and Nobler M.S. The effects of electroconvulsive therapy on quantitative electroencephalograms. Relationship to clinical outcome. Arch. Gen. Psychiatry 53 (1996) 814-824
112. Sanger T.D., Garg R.R., and Chen R. Interactions between two different inhibitory systems in the human motor cortex. J. Physiol. 530 (2001) 307-317
113. Schieber M.H., and Hibbard L.S. How somatotopic is the motor cortex hand area?. Science 261 (1993) 489-492
114. Seamans J.K., Gorelova N., Durstewitz D., and Yang C.R. Bidirectional dopamine modulation of GABAergic inhibition in prefrontal cortical pyramidal neurons. J. Neurosci. 21 (2001) 3628-3638
115. Seeman P., Lee T., Chau-Wong M., and Wong K. Antipsychotic drug doses and neuroleptic/dopamine receptors. Nature 261 (1976) 717-719
116. Selemon L.D., and Goldman-Rakic P.S. The reduced neuropil hypothesis: a circuit based model of schizophrenia [see comments]. Biol. Psychiatry 45 (1999) 17-25
117. Selemon L.D., Rajkowska G., and Goldman-Rakic P.S. Abnormally high neuronal density in the schizophrenic cortex. A morphometric analysis of prefrontal area 9 and occipital area 17. Arch. Gen. Psychiatry 52 (1995) 805-818 (discussion 819-20)
118. Selemon L.D., Rajkowska G., and Goldman-Rakic P.S. Elevated neuronal density in prefrontal area 46 in brains from schizophrenic patients: application of a three-dimensional, stereologic counting method. J. Comp. Neurol. 392 (1998) 402-412
119. Shapley R., Hawken M., and Ringach D.L. Dynamics of orientation selectivity in the primary visual cortex and the importance of cortical inhibition. Neuron 38 (2003) 689-699
120. Siebner H.R., Dressnandt J., Auer C., and Conrad B. Continuous intrathecal baclofen infusions induced a marked increase of the transcranially evoked silent period in a patient with generalized dystonia. Muscle Nerve 21 (1998) 1209-1212
121. Somogyi P., and Cowey A. Combined Golgi and electron microscopic study on the synapses formed by double bouquet cells in the visual cortex of the cat and monkey. J. Comp. Neurol. 195 (1981) 547-566
122. Somogyi P., Freund T.F., and Cowey A. The axo-axonic interneuron in the cerebral cortex of the rat, cat and monkey. Neuroscience 7 (1982) 2577-2607
123. Somogyi P., Tamas G., Lujan R., and Buhl E.H. Salient features of synaptic organisation in the cerebral cortex. Brain Res. Brain Res. Rev. 26 (1998) 113-135
124. Spencer K.M., Nestor P.G., Niznikiewicz M.A., Salisbury D.F., Shenton M.E., and McCarley R.W. Abnormal neural synchrony in schizophrenia. J. Neurosci. 23 (2003) 7407-7411
125. Spencer K.M., Nestor P.G., Perlmutter R., Niznikiewicz M.A., Klump M.C., Frumin M., Shenton M.E., and McCarley R.W. Neural synchrony indexes disordered perception and cognition in schizophrenia. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 17288-17293
126. Sperk G., Furtinger S., Schwarzer C., and Pirker S. GABA and its receptors in epilepsy. Adv. Exp. Med. Biol. 548 (2004) 92-103
127. Stassen H.H., Bridler R., Hagele S., Hergersberg M., Mehmann B., Schinzel A., Weisbrod M., and Scharfetter C. Schizophrenia and smoking: evidence for a common neurobiological basis?. Am. J. Med. Genet. 96 (2000) 173-177
128. Stefansson H., Sigurdsson E., Steinthorsdottir V., Bjornsdottir S., Sigmundsson T., Ghosh S., Brynjolfsson J., Gunnarsdottir S., Ivarsson O., Chou T.T., Hjaltason O., Birgisdottir B., Jonsson H., Gudnadottir V.G., Gudmundsdottir E., Bjornsson A., Ingvarsson B., Ingason A., Sigfusson S., Hardardottir H., Harvey R.P., Lai D., Zhou M., Brunner D., Mutel V., Gonzalo A., Lemke G., Sainz J., Johannesson G., Andresson T., Gudbjartsson D., Manolescu A., Frigge M.L., Gurney M.E., Kong A., Gulcher J.R., Petursson H., and Stefansson K. Neuregulin 1 and susceptibility to schizophrenia. Am. J. Hum. Genet. 71 (2002) 877-892
129. Stevens K.E., Freedman R., Collins A.C., Hall M., Leonard S., Marks M.J., and Rose G.M. Genetic correlation of inhibitory gating of hippocampal auditory evoked response and alpha-bungarotoxin-binding nicotinic cholinergic receptors in inbred mouse strains. Neuropsychopharmacology 15 (1996) 152-162
130. Stevens K.E., Kem W.R., Mahnir V.M., and Freedman R. Selective alpha7-nicotinic agonists normalize inhibition of auditory response in DBA mice. Psychopharmacology (Berl.) 136 (1998) 320-327
131. Stober G., Saar K., Ruschendorf F., Meyer J., Nurnberg G., Jatzke S., Franzek E., Reis A., Lesch K.P., Wienker T.F., and Beckmann H. Splitting schizophrenia: periodic catatonia-susceptibility locus on chromosome 15q15. Am. J. Hum. Genet. 67 (2000) 1201-1207
132. Talbot K., Eidem W.L., Tinsley C.L., Benson M.A., Thompson E.W., Smith R.J., Hahn C.G., Siegel S.J., Trojanowski J.Q., Gur R.E., Blake D.J., and Arnold S.E. Dysbindin-1 is reduced in intrinsic, glutamatergic terminals of the hippocampal formation in schizophrenia. J. Clin. Invest. 113 (2004) 1353-1363
133. Tallon-Baudry C., and Bertrand O. Oscillatory gamma activity in humans and its role in object representation. Trends Cogn. Sci. 3 (1999) 151-162
134. Tsuang D.W., Skol A.D., Faraone S.V., Bingham S., Young K.A., Prabhudesai S., Haverstock S.L., Mena F., Menon A.S., Bisset D., Pepple J., Sauter F., Baldwin C., Weiss D., Collins J., Boehnke M., Schellenberg G.D., and Tsuang M.T. Examination of genetic linkage of chromosome 15 to schizophrenia in a large Veterans Affairs Cooperative Study sample. Am. J. Med. Genet. 105 (2001) 662-668
135. Vinogradova O.S., and Bragin A.G. Sensory characteristics of the cortical input of the hippocampus, the dentate fascia. Zh. Vyssh. Nerv. Deiat. Im. I P Pavlova 25 (1975) 410-420
136. Volz A., Khorsand V., Gillies D., and Leucht S. Benzodiazepines for schizophrenia. Cochrane Database Syst. Rev. (2007) (CD006391)
137. Waldo M., Myles-Worsley M., Madison A., Byerley W., and Freedman R. Sensory gating deficits in parents of schizophrenics. Am. J. Med. Genet. 60 (1995) 506-511
138. Wassermann E.M., Wedegaertner F.R., Ziemann U., George M.S., and Chen R. Crossed reduction of human motor cortex excitability by 1-Hz transcranial magnetic stimulation. Neurosci. Lett. 250 (1998) 141-144
139. Weisser R., Weisbrod M., Roehrig M., Rupp A., Schroeder J., and Scherg M. Is frontal lobe involved in the generation of auditory evoked P50?. NeuroReport 12 (2001) 3303-3307
140. Werhahn K.J., Kunesch E., Noachtar S., Benecke R., and Classen J. Differential effects on motorcortical inhibition induced by blockade of GABA uptake in humans. J. Physiol. (Lond.) 517 (1999) 591-597
141. Whitlock J.R., Heynen A.J., Shuler M.G., and Bear M.F. Learning induces long-term potentiation in the hippocampus. Science 313 (2006) 1093-1097
142. Wolkowitz O.M., Turetsky N., Reus V.I., and Hargreaves W.A. Benzodiazepine augmentation of neuroleptics in treatment-resistant schizophrenia. Psychopharmacol. Bull. 28 (1992) 291-295
143. Woo R.S., Li X.M., Tao Y., Carpenter-Hyland E., Huang Y.Z., Weber J., Neiswender H., Dong X.P., Wu J., Gassmann M., Lai C., Xiong W.C., Gao T.M., and Mei L. Neuregulin-1 enhances depolarization-induced GABA release. Neuron 54 (2007) 599-610
144. Xu J., Pato M.T., Torre C.D., Medeiros H., Carvalho C., Basile V.S., Bauer A., Dourado A., Valente J., Soares M.J., Macedo A.A., Coelho I., Ferreira C.P., Azevedo M.H., Macciardi F., Kennedy J.L., and Pato C.N. Evidence for linkage disequilibrium between the alpha 7-nicotinic receptor gene (CHRNA7) locus and schizophrenia in Azorean families. Am. J. Med. Genet. 105 (2001) 669-674
145. Yang L., Long C., and Faingold C.L. Audiogenic seizure susceptibility is induced by termination of continuous infusion of gamma-aminobutyric acid or an N-methyl-d-aspartic acid antagonist into the inferior colliculus. Exp. Neurol. 171 (2001) 147-152
146. Yee B.K., Keist R., von Boehmer L., Studer R., Benke D., Hagenbuch N., Dong Y., Malenka R.C., Fritschy J.M., Bluethmann H., Feldon J., Mohler H., and Rudolph U. A schizophrenia-related sensorimotor deficit links alpha 3-containing GABAA receptors to a dopamine hyperfunction. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 17154-17159
147. Zai G., King N., Wong G.W., Barr C.L., and Kennedy J.L. Possible association between the gamma-aminobutyric acid type B receptor 1 (GABBR1) gene and schizophrenia. Eur. Neuropsychopharmacol. 15 (2005) 347-352
148. Ziemann U., Bruns D., and Paulus W. Impaired motor cortex inhibition in patients with Parkinson's disease and other parkinsonian syndromes. A transcranial magnetic stimulation study [abstract]. Mov. Disord. 11 (1996) 72
149. Ziemann U., Lonnecker S., Steinhoff B.J., and Paulus W. The effect of lorazepam on the motor cortical excitability in man. Exp. Brain Res. 109 (1996) 127-135