EEG biomarkers of target engagement, therapeutic effect, and disease process

Annals of the New York Academy of Sciences

Volumn 1344, Issue 1, 2015, Pages 12-26

  Featherstone, Robert E ^a   Mcmullen, Mary F ^a   Ward, Katelyn R ^a   Bang, Jakyung ^a   Xiao, Jane ^a   Siegel, Steven J ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

EEG; NMDA; Schizophrenia

Indexed keywords

4 AMINOBUTYRIC ACID B RECEPTOR STIMULATING AGENT; BIOLOGICAL MARKER; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PARVALBUMIN; 4 AMINOBUTYRIC ACID B RECEPTOR;

ALPHA RHYTHM; ANIMAL BEHAVIOR; ARTICLE; BETA RHYTHM; COGNITION; DELTA RHYTHM; DISEASE COURSE; ELECTROENCEPHALOGRAM; ELECTROENCEPHALOGRAPHY; EVENT RELATED POTENTIAL; EVOKED BRAIN STEM AUDITORY RESPONSE; GAMMA RHYTHM; HUMAN; IN VITRO STUDY; INTERNEURON; MENTAL PATIENT; MISMATCH NEGATIVITY; MOUSE MODEL; NERVE CELL; NERVE CELL EXCITABILITY; NONHUMAN; OSCILLATION; PATCH CLAMP TECHNIQUE; PSYCHOPHARMACOTHERAPY; PYRAMIDAL NERVE CELL; SCHIZOPHRENIA; SOCIAL INTERACTION; SOCIAL STATUS; TASK PERFORMANCE; THERAPY EFFECT; THETA RHYTHM; TRANSGENIC MOUSE; ANIMAL; DISEASE MODEL; EVOKED RESPONSE; METABOLISM; MOUSE; PATHOPHYSIOLOGY; TRANSLATIONAL RESEARCH;

ANIMALIA; MUS; MUS MUSCULUS;

ANIMALS; BEHAVIOR, ANIMAL; BIOLOGICAL MARKERS; DISEASE MODELS, ANIMAL; ELECTROENCEPHALOGRAPHY; EVOKED POTENTIALS; GABA-B RECEPTOR AGONISTS; HUMANS; MICE; RECEPTORS, GABA-B; RECEPTORS, N-METHYL-D-ASPARTATE; SCHIZOPHRENIA; TRANSLATIONAL MEDICAL RESEARCH;

EID: 84928231943     PISSN: 00778923     EISSN: 17496632     Source Type: Book Series    
DOI: 10.1111/nyas.12745     Document Type: Article

References (160)

1. Berger, H. 1929. Ueber das Electrocephalogramm des Menschen. Arch. Psychiatr. Nervenkr. 87: 527-570.
2. Dietrich, A. & R. Kanso . 2010. A review of EEG, ERP, and neuroimaging studies of creativity and insight. Psychol. Bull. 136: 822-848.
3. Gandal, M.J. et al. 2012. Gamma synchrony: towards a translational biomarker for the treatment-resistant symptoms of schizophrenia. Neuropharmacology 62: 1504-1518.
4. Basar, E. et al. 2001. Gamma, alpha, delta, and theta oscillations govern cognitive processes. Int. J. Psychophysiol. 39: 241-248.
5. Roach, B.J. & D.H. Mathalon . 2008. Event-related EEG time-frequency analysis: an overview of measures and an analysis of early gamma band phase locking in schizophrenia. Schizophr. Bull. 34: 907-926.
6. Ranlund, S. et al. 2014. Resting EEG in psychosis and at-risk populations-a possible endophenotype? Schizophr. Res. 153: 96-102.
7. Boutros, N.N. et al. 2008. The status of spectral EEG abnormality as a diagnostic test for schizophrenia. Schizophr. Res. 99: 225-237.
8. Doege, K. et al. 2009. Reduced event-related low frequency EEG activity in schizophrenia during an auditory oddball task. Psychophysiology 46: 566-577.
9. Siekmeier, P.J. & S.M. Stufflebeam . 2010. Patterns of spontaneous magnetoencephalographic activity in patients with schizophrenia. J. Clin. Neurophysiol. 27: 179-190.
10. Buzsaki, G. 2002. Theta oscillations in the hippocampus. Neuron 33: 325-340.
11. Hong, L.E. et al. 2012. A shared low-frequency oscillatory rhythm abnormality in resting and sensory gating in schizophrenia. Clin. Neurophysiol. 123: 285-292.
12. Bates, A.T. et al. 2009. Low-frequency EEG oscillations associated with information processing in schizophrenia. Schizophr. Res. 115: 222-230.
13. Hamm, J.P. et al. 2011. Abnormalities of neuronal oscillations and temporal integration to low- and high-frequency auditory stimulation in schizophrenia. Biol. Psychiatry 69: 989-996.
14. Jacobs, J. et al. 2006. EEG oscillations and recognition memory: theta correlates of memory retrieval and decision making. Neuroimage 32: 978-987.
15. Lega, B.C., J. Jacobs & M. Kahana . 2012. Human hippocampal theta oscillations and the formation of episodic memories. Hippocampus 22: 748-761.
16. Osipova, D. et al. 2006. Theta and gamma oscillations predict encoding and retrieval of declarative memory. J. Neurosci. 26: 7523-7531.
17. Tesche, C.D. & J. Karhu . 2000. Theta oscillations index human hippocampal activation during a working memory task. Proc. Natl. Acad. Sci. U.S.A. 97: 919-924.
18. Schmiedt, C. et al. 2005. Event-related theta oscillations during working memory tasks in patients with schizophrenia and healthy controls. Brain Res. Cogn. Brain Res. 25: 936-947.
19. Benchenane, K. et al. 2010. Coherent theta oscillations and reorganization of spike timing in the hippocampal- prefrontal network upon learning. Neuron 66: 921-936.
20. Colgin, L.L. 2011. Oscillations and hippocampal-prefrontal synchrony. Curr. Opin. Neurobiol. 21: 467-474.
21. Fujisawa, S. & G. Buzsaki . 2011. A 4 Hz oscillation adaptively synchronizes prefrontal, VTA, and hippocampal activities. Neuron 72: 153-165.
22. Gordon, J.A. 2011. Oscillations and hippocampal-prefrontal synchrony. Curr. Opin. Neurobiol. 21: 486-491.
23. Sigurdsson, T. et al. 2010. Impaired hippocampal-prefrontal synchrony in a genetic mouse model of schizophrenia. Nature 464: 763-767.
24. Brenner, C.A. et al. 2009. Steady state responses: electrophysiological assessment of sensory function in schizophrenia. Schizophr. Bull. 35: 1065-1077.
25. Sponheim, S.R. et al. 1994. Resting EEG in first-episode and chronic schizophrenia. Psychophysiology 31: 37-43.
26. Merrin, E.L. & T.C. Floyd . 1992. Negative symptoms and EEG alpha activity in schizophrenic patients. Schizophr. Res. 8: 11-20.
27. Merrin, E.L. & T.C. Floyd . 1996. Negative symptoms and EEG alpha in schizophrenia: a replication. Schizophr. Res. 19: 151-161.
28. Boutros, N.N. et al. 2014. Negative symptoms in schizophrenia. Clin. Schizophr. Relat. Psychoses. 8: 28-35B.
29. Boutros, N.N. et al. 2014. Electrophysiological aberrations associated with negative symptoms in schizophrenia. Curr. Top. Behav. Neurosci. 21: 129-156.
30. Haenschel, C. et al. 2009. Cortical oscillatory activity is critical for working memory as revealed by deficits in early-onset schizophrenia. J. Neurosci. 29: 9481-9489.
31. Gallinat, J. et al. 2004. Reduced oscillatory gamma-band responses in unmedicated schizophrenic patients indicate impaired frontal network processing. Clin. Neurophysiol. 115: 1863-1874.
32. Makeig, S., T.P. Jung & T.J. Sejnowski . 2000. Awareness during drowsiness: dynamics and electrophysiological correlates. Can. J. Exp. Psychol. 54: 266-273.
33. Kopell, N. et al. 2000. Gamma rhythms and beta rhythms have different synchronization properties. Proc. Natl. Acad. Sci. U.S.A. 97: 1867-1872.
34. Rutter, L. et al. 2009. Magnetoencephalographic gamma power reduction in patients with schizophrenia during resting condition. Hum. Brain Mapp. 30: 3254-3264.
35. Uhlhaas, P.J. et al. 2006. Dysfunctional long-range coordination of neural activity during Gestalt perception in schizophrenia. J. Neurosci. 26: 8168-8175.
36. Symond, M.P. et al. 2005. "Gamma synchrony" in first-episode schizophrenia: a disorder of temporal connectivity? Am. J. Psychiatry 162: 459-465.
37. Leicht, G. et al. 2010. Reduced early auditory evoked gamma-band response in patients with schizophrenia. Biol. Psychiatry 67: 224-231.
38. Fuchs, E.C. et al. 2001. Genetically altered AMPA-type glutamate receptor kinetics in interneurons disrupt long-range synchrony of gamma oscillation. Proc. Natl. Acad. Sci. U.S.A. 98: 3571-3576.
39. Sohal, V.S. et al. 2009. Parvalbumin neurons and gamma rhythms enhance cortical circuit performance. Nature 459: 698-702.
40. Cardin, J.A. et al. 2009. Driving fast-spiking cells induces gamma rhythm and controls sensory responses. Nature 459: 663-667.
41. Traub, R.D. et al. 1996. A mechanism for generation of long-range synchronous fast oscillations in the cortex. Nature 383: 621-624.
42. Uhlhaas, P.J. et al. 2010. Neural synchrony and the development of cortical networks. Trends Cogn. Sci. 14: 72-80.
43. Billingslea, E.N. et al. 2014. Parvalbumin cell ablation of NMDA-R1 causes increased resting network excitability with associated social and self-care deficits. Neuropsychopharmacology 39: 1603-1613.
44. Tatard-Leitman, V.M. et al. 2015. Pyramidal cell selective ablation of N-methyl-d-aspartate receptor 1 causes increase in cellular and network excitability. Biol. Psychiatry 77: 556-568.
45. Ehrlichman, R.S. et al. 2009. Neuregulin 1 transgenic mice display reduced mismatch negativity, contextual fear conditioning and social interactions. Brain Res. 1294: 116-127.
46. Gandal, M.J. et al. 2008. A novel electrophysiological model of chemotherapy-induced cognitive impairments in mice. Neuroscience 157: 95-104.
47. Lazarewicz, M.T. et al. 2010. Ketamine modulates theta and gamma oscillations. J. Cogn. Neurosci. 22: 1452-1464.
48. Saunders, J.A., M.J. Gandal & S.J. Siegel . 2012. NMDA antagonists recreate signal-to-noise ratio and timing perturbations present in schizophrenia. Neurobiol. Dis. 46: 93-100.
49. Henry, K.R. 1979. Auditory brainstem volume-conducted responses: origins in the laboratory mouse. J. Am. Aud. Soc. 4: 173-178.
50. Skold, M. et al. 2014. Thalamocortical abnormalities in auditory brainstem response patterns distinguish DSM-IV bipolar disorder type I from schizophrenia. J. Affect. Disord. 169: 105-111.
51. Tarasenko, M.A. et al. 2014. The auditory brain-stem response to complex sounds: a potential biomarker for guiding treatment of psychosis. Front. Psychiatry 5: 142.
52. Korzyukov, O. et al. 2007. Generators of the intracranial P50 response in auditory sensory gating. Neuroimage 35: 814-826.
53. Picton, T.W. et al. 1974. Human auditory evoked potentials. I. Evaluation of components. Electroencephalogr. Clin. Neurophysiol. 36: 179-190.
54. Cullum, C.M. et al. 1993. Neurophysiological and neuropsychological evidence for attentional dysfunction in schizophrenia. Schizophr. Res. 10: 131-141.
55. Erwin, R.J. et al. 1998. P50 abnormalities in schizophrenia: relationship to clinical and neuropsychological indices of attention. Schizophr. Res. 33: 157-167.
56. Potter, D. et al. 2006. Review of clinical correlates of P50 sensory gating abnormalities in patients with schizophrenia. Schizophr Bull. 32: 692-700.
57. deWilde, O.M. et al. 2007. A meta-analysis of P50 studies in patients with schizophrenia and relatives: differences in methodology between research groups. Schizophr. Res. 97: 137-151.
58. Light, G.A. & D.L. Braff . 1998. The "incredible shrinking" P50 event-related potential. Biol. Psychiatry 43: 918-920.
59. Lamberti, J.S. et al. 1993. Within-session changes in sensory gating assessed by P50 evoked potentials in normal subjects. Prog. Neuropsychopharmacol. Biol. Psychiatry 17: 781-791.
60. Turetsky, B.I. et al. 2009. Profile of auditory information-processing deficits in schizophrenia. Psychiatry Res. 165: 27-37.
61. Ahveninen, J. et al. 2006. Inherited auditory-cortical dysfunction in twin pairs discordant for schizophrenia. Biol. Psychiatry 60: 612-620.
62. Rosburg, T. et al. 2009. Sensory gating in intracranial recordings-the role of phase locking. Neuroimage 44: 1041-1049.
63. Rosburg, T. et al. 2004. Short-term habituation of the intracranially recorded auditory evoked potentials P50 and N100. Neurosci. Lett. 372: 245-249.
64. Boutros, N.N. et al. 2009. Sensory-gating deficit of the N100 mid-latency auditory evoked potential in medicated schizophrenia patients. Schizophr. Res. 113: 339-346.
65. Boutros, N.N. et al. 2004. Morphological and latency abnormalities of the mid-latency auditory evoked responses in schizophrenia: a preliminary report. Schizophr. Res. 70: 303-313.
66. Boutros, N.N. et al. 2004. Sensory gating deficits during the mid-latency phase of information processing in medicated schizophrenia patients. Psychiatry Res. 126: 203-215.
67. Jansen, B.H., A. Hegde & N.N. Boutros . 2004. Contribution of different EEG frequencies to auditory evoked potential abnormalities in schizophrenia. Clin. Neurophysiol. 115: 523-533.
68. Laurent, A. et al. 1999. Auditory event-related potentials and clinical scores in unmedicated schizophrenic patients. Psychiatry Res. 86: 229-238.
69. Strik, W.K. et al. 1992. Disorders of smooth pursuit eye movement and auditory N100 in schizophrenic patients. Psychiatry Res. 41: 227-235.
70. Frangou, S. et al. 1997. The Maudsley Family Study, II: Endogenous event-related potentials in familial schizophrenia. Schizophr. Res. 23: 45-53.
71. Blackwood, D.H. et al. 1991. Auditory P300 and eye tracking dysfunction in schizophrenic pedigrees. Arch. Gen. Psychiatry 48: 899-909.
72. Lijffijt, M. et al. 2009. P50, N100, and P200 sensory gating: relationships with behavioral inhibition, attention, and working memory. Psychophysiology 46: 1059-1068.
73. Turetsky, B.I. et al. 2008. Abnormal auditory N100 amplitude: a heritable endophenotype in first-degree relatives of schizophrenia probands. Biol. Psychiatry 64: 1051-1059.
74. Roth, W.T. et al. 1981. Auditory event-related potentials in schizophrenia and depression. Psychiatry Res. 4: 199-212.
75. Murck, H. et al. 2006. Hypericum extract reverses S-ketamine-induced changes in auditory evoked potentials in humans-possible implications for the treatment of schizophrenia. Biol. Psychiatry 59: 440-445.
76. Umbricht, D. & S. Krljes . 2005. Mismatch negativity in schizophrenia: a meta-analysis. Schizophr. Res. 76: 1-23.
77. Javitt, D.C. 2008. Phenomenology, aetiology and treatment of schizophrenia. Novartis Found. Symp. 289: 4-16; discussion 17-22, 87-93.
78. Shelley, A.M. et al. 1991. The effect of repeated testing on ERP components during auditory selective attention. Psychophysiology 28: 496-510.
79. Naatanen, R., T. Jacobsen & I. Winkler . 2005. Memory-based or afferent processes in mismatch negativity (MMN): a review of the evidence. Psychophysiology 42: 25-32.
80. Light, G.A. & D.L. Braff . 2005. Mismatch negativity deficits are associated with poor functioning in schizophrenia patients. Arch. Gen. Psychiatry 62: 127-136.
81. Light, G.A., N.R. Swerdlow & D.L. Braff . 2007. Preattentive sensory processing as indexed by the MMN and P3a brain responses is associated with cognitive and psychosocial functioning in healthy adults. J. Cogn. Neurosci. 19: 1624-1632.
82. Baldeweg, T. et al. 2004. Mismatch negativity potentials and cognitive impairment in schizophrenia. Schizophr. Res. 69: 203-217.
83. Javitt, D.C. et al. 1995. Impaired mismatch negativity generation reflects widespread dysfunction of working memory in schizophrenia. Arch. Gen. Psychiatry 52: 550-558.
84. Sevik, A.E. et al. 2011. Neuropsychological performance and auditory event related potentials in schizophrenia patients and their siblings: a family study. Schizophr Res. 130: 195-202.
85. Javitt, D.C. 2000. Intracortical mechanisms of mismatch negativity dysfunction in schizophrenia. Audiol. Neurootol. 5: 207-215.
86. Javitt, D.C. et al. 1996. Role of cortical N-methyl-D-aspartate receptors in auditory sensory memory and mismatch negativity generation: implications for schizophrenia. Proc. Natl. Acad. Sci. U.S.A. 93: 11962-11967.
87. Ehrlichman, R.S. et al. 2008. Deviance-elicited changes in event-related potentials are attenuated by ketamine in mice. J. Cogn. Neurosci. 20: 1403-1414.
88. Umbricht, D. et al. 2000. Ketamine-induced deficits in auditory and visual context-dependent processing in healthy volunteers: implications for models of cognitive deficits in schizophrenia. Arch. Gen. Psychiatry 57: 1139-1147.
89. Linden, D.E. 2005. The p300: where in the brain is it produced and what does it tell us? Neuroscientist 11: 563-576.
90. Polich, J. 2007. Updating P300: an integrative theory of P3a and P3b. Clin. Neurophysiol. 118: 2128-2148.
91. Devrim-Ucok, M., H.Y. Keskin-Ergen & A. Ucok . 2006. Novelty P3 and P3b in first-episode schizophrenia and chronic schizophrenia. Prog. Neuropsychopharmacol. Biol. Psychiatry 30: 1426-1434.
92. vander Stelt, O. & G.J. vanBoxtel . 2008. Auditory P300 and mismatch negativity in comatose states. Clin. Neurophysiol. 119: 2172-2174.
93. Alain, C. et al. 2002. Deficits in automatically detecting changes in conjunction of auditory features in patients with schizophrenia. Psychophysiology 39: 599-606.
94. Mathalon, D.H., J.M. Ford & A. Pfefferbaum . 2000. Trait and state aspects of P300 amplitude reduction in schizophrenia: a retrospective longitudinal study. Biol. Psychiatry 47: 434-449.
95. Mathalon, D.H. et al. 2010. Neurophysiological distinction between schizophrenia and schizoaffective disorder. Front. Hum. Neurosci. 3: 70.
96. Ford, J. 2008. 2008 in review: more growing pains. Twinges as the NP role expands. Adv. Nurse Pract. 16: 56-57.
97. Frodl, T. et al. 2001. Corpus callosum and P300 in schizophrenia. Schizophr. Res. 49: 107-119.
98. Mathalon, D.H. et al. 2000. P300 reduction and prolongation with illness duration in schizophrenia. Biol. Psychiatry 47: 413-427.
99. Hansch, E.C. et al. 1982. Cognition in Parkinson disease: an event-related potential perspective. Ann. Neurol. 11: 599-607.
100. Stanzione, P. et al. 1991. P300 variations in parkinsonian patients before and during dopaminergic monotherapy: a suggested dopamine component in P300. Electroencephalogr. Clin. Neurophysiol. 80: 446-453.
101. Watson, T.D. et al. 2009. Modulation of the cortical processing of novel and target stimuli by drugs affecting glutamate and GABA neurotransmission. Int. J. Neuropsychopharmacol. 12: 357-370.
102. Barcelo, F., J.A. Perianez & E. Nyhus . 2007. An information theoretical approach to task-switching: evidence from cognitive brain potentials in humans. Front. Hum. Neurosci. 1: 13.
103. Squires, K.C. & E. Donchin . 1976. Beyond averaging: the use of discriminant functions to recognize event related potentials elicited by single auditory stimuli. Electroencephalogr. Clin. Neurophysiol. 41: 449-459.
104. Bramon, E. et al. 2004. Meta-analysis of the P300 and P50 waveforms in schizophrenia. Schizophr. Res. 70: 315-329.
105. Coburn, K.L. et al. 1998. P300 delay and attenuation in schizophrenia: reversal by neuroleptic medication. Biol. Psychiatry 44: 466-474.
106. Roxborough, H. et al. 1993. Neuropsychological and P300 abnormalities in schizophrenics and their relatives. Psychol. Med. 23: 305-314.
107. Pfefferbaum, A. et al. 1989. P3 in schizophrenia is affected by stimulus modality, response requirements, medication status, and negative symptoms. Arch. Gen. Psychiatry 46: 1035-1044.
108. Pritchard, W.S. et al. 1986. No decrement in visual P300 amplitude during extended performance of the oddball task. Int. J. Neurosci. 29: 199-204.
109. Martin-Loeches, M. et al. 2001. P300 amplitude as a possible correlate of frontal degeneration in schizophrenia. Schizophr. Res. 49: 121-128.
110. Olichney, J.M. et al. 1998. Relationship between auditory P300 amplitude and age of onset of schizophrenia in older patients. Psychiatry Res. 79: 241-254.
111. Kidogami, Y. et al. 1991. P300 in first degree relatives of schizophrenics. Schizophr. Res. 6: 9-13.
112. Saitoh, O. et al. 1984. Abnormalities in late positive components of event-related potentials may reflect a genetic predisposition to schizophrenia. Biol. Psychiatry 19: 293-303.
113. Rissling, A.J. et al. 2012. Disentangling early sensory information processing deficits in schizophrenia. Clin. Neurophysiol. 123: 1942-1949.
114. Rissling, A.J. et al. 2014. Cortical substrates and functional correlates of auditory deviance processing deficits in schizophrenia. Neuroimage Clin. 6: 424-437.
115. Brunia, C.H. et al. 2011. Waiting to perceive: reward or punishment? Clin. Neurophysiol. 122: 858-868.
116. Halene, T.B. & S.J. Siegel . 2008. Antipsychotic-like properties of phosphodiesterase 4 inhibitors: evaluation of 4-(3-butoxy-4-methoxybenzyl)-2-imidazolidinone (RO-20-1724) with auditory event-related potentials and prepulse inhibition of startle. J. Pharmacol. Exp. Ther. 326: 230-239.
117. Connolly, P.M. et al. 2004. The effects of ketamine vary among inbred mouse strains and mimic schizophrenia for the P80, but not P20 or N40 auditory ERP components. Neurochem. Res. 29: 1179-1188.
118. Maxwell, C.R. et al. 2006. Ketamine produces lasting disruptions in encoding of sensory stimuli. J. Pharmacol. Exp. Ther. 316: 315-324.
119. Metzger, K.L. et al. 2007. Effects of nicotine vary across two auditory evoked potentials in the mouse. Biol. Psychiatry 61: 23-30.
120. Phillips, J.M., R.S. Ehrlichman & S.J. Siegel . 2007. Mecamylamine blocks nicotine-induced enhancement of the P20 auditory event-related potential and evoked gamma. Neuroscience 144: 1314-1323.
121. Rudnick, N.D. et al. 2009. Role of beta2-containing nicotinic acetylcholine receptors in auditory event-related potentials. Psychopharmacology (Berl.) 202: 745-751.
122. Siegel, S.J. et al. 2005. Monoamine reuptake inhibition and nicotine receptor antagonism reduce amplitude and gating of auditory evoked potentials. Neuroscience 133: 729-738.
123. Adler, L.E. et al. 1988. Modulation of the gating of auditory evoked potentials by norepinephrine: pharmacological evidence obtained using a selective neurotoxin. Biol. Psychiatry 24: 179-190.
124. Freedman, R. et al. 1987. Neurobiological studies of sensory gating in schizophrenia. Schizophr. Bull. 13: 669-678.
125. Maxwell, C.R. et al. 2004. Phosphodiesterase inhibitors: a novel mechanism for receptor-independent antipsychotic medications. Neuroscience 129: 101-107.
126. Rudnick, N.D. et al. 2010. Mouse model predicts effects of smoking and varenicline on event-related potentials in humans. Nicotine Tob. Res. 12: 589-597.
127. Stevens, K.E. et al. 1996. Genetic correlation of inhibitory gating of hippocampal auditory evoked response and alpha-bungarotoxin-binding nicotinic cholinergic receptors in inbred mouse strains. Neuropsychopharmacology 15: 152-162.
128. Stevens, K.E. & K.D. Wear . 1997. Normalizing effects of nicotine and a novel nicotinic agonist on hippocampal auditory gating in two animal models. Pharmacol. Biochem. Behav. 57: 869-874.
129. Freedman, R. et al. 1997. Linkage of a neurophysiological deficit in schizophrenia to a chromosome 15 locus. Proc. Natl. Acad. Sci. U.S.A. 94: 587-592.
130. Featherstone, R.E. et al. 2012. Nicotine receptor subtype-specific effects on auditory evoked oscillations and potentials. PLoS One 7: e39775.
131. Boutros, N.N., G. Zouridakis & J. Overall . 1991. Replication and extension of P50 findings in schizophrenia. Clin. Electroencephalogr. 22: 40-45.
132. Gjini, K. et al. 2013. Evoked potential correlates of post-traumatic stress disorder in refugees with history of exposure to torture. J. Psychiatr. Res. 47: 1492-1498.
133. Jin, Y. et al. 1997. Effects of P50 temporal variability on sensory gating in schizophrenia. Psychiatry Res. 70: 71-81.
134. Ehrlichman, R.S. et al. 2009. N-methyl-d-aspartic acid receptor antagonist-induced frequency oscillations in mice recreate pattern of electrophysiological deficits in schizophrenia. Neuroscience 158: 705-712.
135. Siegel, S.J. et al. 2003. Effects of strain, novelty, and NMDA blockade on auditory-evoked potentials in mice. Neuropsychopharmacology 28: 675-682.
136. Bickford-Wimer, P.C. et al. 1990. Auditory sensory gating in hippocampal neurons: a model system in the rat. Biol. Psychiatry 27: 183-192.
137. Koenig, J.I. et al. 2005. Prenatal exposure to a repeated variable stress paradigm elicits behavioral and neuroendocrinological changes in the adult offspring: potential relevance to schizophrenia. Behav. Brain Res. 156: 251-261.
138. Maxwell, C.R. et al. 2006. Mice expressing constitutively active Gsalpha exhibit stimulus encoding deficits similar to those observed in schizophrenia patients. Neuroscience 141: 1257-1264.
139. Cao, Y.A. et al. 2012. Nicotine normalizes event related potentials in COMT-Val-tg mice and increases gamma and theta spectral density. Behav. Neurosci. 126: 332-343.
140. Featherstone, R.E. et al. 2012. Subchronic ketamine treatment leads to permanent changes in EEG, cognition and the astrocytic glutamate transporter EAAT2 in mice. Neurobiol. Dis. 47: 338-346.
141. Amann, L.C. et al. 2009. Chronic ketamine impairs fear conditioning and produces long-lasting reductions in auditory evoked potentials. Neurobiol. Dis. 35: 311-317.
142. Tunbridge, E.M., P.J. Harrison & D.R. Weinberger . 2006. Catechol-o-methyltransferase, cognition, and psychosis: Val158Met and beyond. Biol. Psychiatry 60: 141-151.
143. Meyer-Lindenberg, A. et al. 2005. Midbrain dopamine and prefrontal function in humans: interaction and modulation by COMT genotype. Nat. Neurosci. 8: 594-596.
144. Papaleo, F. et al. 2008. Genetic dissection of the role of catechol-O-methyltransferase in cognition and stress reactivity in mice. J. Neurosci. 28: 8709-8723.
145. Golimbet, V. et al. 2006. Association study of COMT gene Val158Met polymorphism with auditory P300 and performance on neurocognitive tests in patients with schizophrenia and their relatives. World J. Biol. Psychiatry 7: 238-245.
146. Gallinat, J. et al. 2003. Association of the G1947A COMT (Val(108/158)Met) gene polymorphism with prefrontal P300 during information processing. Biol. Psychiatry 54: 40-48.
147. Bickel, S. & D.C. Javitt . 2009. Neurophysiological and neurochemical animal models of schizophrenia: focus on glutamate. Behav. Brain Res. 204: 352-362.
148. Bickel, S., H.P. Lipp & D. Umbricht . 2007. Impaired attentional modulation of auditory evoked potentials in N-methyl-d-aspartate NR1 hypomorphic mice. Genes Brain Behav. 6: 558-568.
149. Bickel, S., H.P. Lipp & D. Umbricht . 2008. Early auditory sensory processing deficits in mouse mutants with reduced NMDA receptor function. Neuropsychopharmacology 33: 1680-1689.
150. Criado, J.R. & C.L. Ehlers . 2009. Event-related oscillations as risk markers in genetic mouse models of high alcohol preference. Neuroscience 163: 506-523.
151. Ehlers, C.L. & C. Somes . 2002. Long latency event-related potentials in mice: effects of stimulus characteristics and strain. Brain Res. 957: 117-128.
152. Ehlers, C.L. et al. 1999. Neurontensin studies in alcohol naive, preferring and non-preferring rats. Neuroscience 93: 227-236.
153. Slawecki, C.J. et al. 2003. EEG and ERP profiles in the high alcohol preferring (HAP) and low alcohol preferring (LAP) mice: relationship to ethanol preference. Brain Res. 961: 243-254.
154. Grupe, M. et al. 2014. Neuropharmacological modulation of the P3-like event-related potential in a rat two-tone auditory discrimination task with modafinil and NS9283, a positive allosteric modulator of alpha4beta2 nAChRs. Neuropharmacology 79: 444-455.
155. Laursen, B. et al. 2014. Hippocampal P3-like auditory event-related potentials are disrupted in a rat model of cholinergic degeneration in Alzheimer's disease: reversal by donepezil treatment. J. Alzheimer's Dis. 42: 1179-1189.
156. Moessnang, C. et al. 2012. The electrophysiological signature of motivational salience in mice and implications for schizophrenia. Neuropsychopharmacology 37: 2846-2854.
157. Behrens, M.M., S.S. Ali & L.L. Dugan . 2008. Interleukin-6 mediates the increase in NADPH-oxidase in the ketamine model of schizophrenia. J. Neurosci. 28: 13957-13966.
158. Lodge, D.J., M.M. Behrens & A.A. Grace . 2009. A loss of parvalbumin-containing interneurons is associated with diminished oscillatory activity in an animal model of schizophrenia. J. Neurosci. 29: 2344-2354.
159. Amann, L.C. et al. 2010. Mouse behavioral endophenotypes for schizophrenia. Brain Res. Bull. 83: 147-161.
160. Featherstone, R.E., R. Shin, J.H. Kogan, et al. 2015. Mice with subtle reduction of NMDA NR1 receptor subunit expression have a selective decrease in mismatch negativity: implications for schizophrenia prodromal population. Neurobiol. Dis. 73: 289-295.