Reduction of Prelimbic Inhibitory Gating of Auditory Evoked Potentials After Fear Conditioning

Behavioral Neuroscience

Volumn 123, Issue 2, 2009, Pages 315-327

  Mears, Ryan P ^a   Boutros, Nash N ^a   Cromwell, Howard C ^b  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b BOWLING GREEN STATE UNIVERSITY   (United States)

Author keywords

acute stress; evoked potentials; negative affect; prefrontal cortex; sensory gating

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; AUDITORY STIMULATION; BEHAVIORAL SCIENCE; CONTROLLED STUDY; ELECTRIC POTENTIAL; EVOKED AUDITORY RESPONSE; FEAR; INHIBITORY GATING; LIMBIC CORTEX; MALE; NERVOUS SYSTEM FUNCTION; NONHUMAN; ORIENTING RESPONSE; PREFRONTAL CORTEX; RAT; STIMULUS RESPONSE;

ACOUSTIC STIMULATION; ANIMALS; CONDITIONING, CLASSICAL; ELECTROENCEPHALOGRAPHY; ELECTROSHOCK; EVOKED POTENTIALS, AUDITORY; EXTINCTION, PSYCHOLOGICAL; FEAR; MALE; NEURAL INHIBITION; PREFRONTAL CORTEX; RATS; RATS, SPRAGUE-DAWLEY; REACTION TIME; SENSORY GATING; STATISTICS, NONPARAMETRIC;

EID: 65249087902     PISSN: 07357044     EISSN: None     Source Type: Journal    
DOI: 10.1037/a0014364     Document Type: Article

References (95)

1. Abercrombie E.D., Keefe K.A., DiFrischia D.S., and Zigmond M.J. Differential effect of stress on in vivo dopamine release in striatum, nucleus accumbens, and medial frontal cortex. Journal of Neurochemistry 52 (1989) 1655-1658
2. Adler L.E., Olincey A., Cawthra E., Hoffer M., Nagamoto H.T., Amass L., and Freedman R. Reversal of diminished inhibitory sensory gating in cocaine addicts by a nicotinic cholinergic mechanism. Neuropsychopharmacology 24 (2001) 671-679
3. Adler L.E., Pachtman E., Franks R., Pecevich M., Waldo M.C., and Freedman R. Neurophysiological evidence for a defect in neuronal mechanisms involved in sensory gating in schizophrenia. Biological Psychiatry 17 (1982) 639-654
4. Adler L.E., Rose G., and Freedman R. Neurophysiological studies of sensory gating in rats: Effects of amphetamine, phencyclidine, and haloperidol. Biological Psychiatry 21 (1986) 787-798
5. Adler L.E., Waldo M.C., Tatcher A., Cawthra E., Baker N., and Freedman R. Lack of relationship of auditory gating defects to negative symptoms in schizophrenia. Schizophrenia Research 3 2 (1990) 131-138
6. Arnsten A.F. The biology of being frazzled. Science 280 5370 (1998) 1711-1712
7. Arnsten A.F., and Goldman-Rakic P.S. Noise stress impairs prefrontal cortical cognitive function in monkeys: Evidence for a hyperdopaminergic mechanism. Archives of General Psychiatry 55 (1998) 362-368
8. Berridge K.C., and Cromwell H.C. Motivational-sensorimotor interaction controls aphagia and exaggerated treading after striatopallidal lesions. Behavioral Neuroscience 104 (1990) 778-795
9. Bickford P.C., Luntz-Leybman V., and Freedman R. Auditory sensory gating in the rat hippocampus: Modulation by brainstem activity. Brain Research 607 (1993) 33-38
10. Bickford-Wimer P.A., Nagamoto H.T., Johnson R., Adler L.E., Egan M., Rose G., et al. Auditory sensory gating in hippocampal neurons: A model system in the rat. Biological Psychiatry 27 (1990) 183-192
11. Birrell J.M., and Brown V.J. Medial frontal cortex mediates perceptual attentional set shifting in the rat. Journal of Neuroscience 20 (2000) 4320-4324
12. Bock G., and Goode J. Sodium channels and neuronal hyperexcitability (2002), Wiley, Chichester, England
13. Boutros N.N., and Belger A. Midlatency evoked potentials attenutaion and augmentation reflect different aspects of sensory gating. Biological Psychiatry 45 (1999) 917-922
14. Boutros N.N., Gelernter J., Gooding D.C., Cubells J., Young A., Krystal J.H., et al. Sensory gating and psychosis vulnerability in cocaine-dependent individuals: Preliminary data. Biological Psychiatry 51 (2002) 683-686
15. Boutros N.N., Korzyukov O., Jansen B., Feingold A., and Bell M. Sensory gating deficits during the mid-latency phase of information processing in medicated schizophrenia patients. Psychiatry Research 126 (2004) 203-215
16. Boutros N.N., and Kwan S.W. Test-retest reliability of the rat N40 auditory evoked response: Preliminary data. Psychiatry Research 81 (1998) 269-276
17. Boutros N.N., Mears R., Pflieger M.E., Moxon K.A., Ludowig E., and Rosburg T. Sensory gating in the human hippocampal and rhinal regions: Regional differences. Hippocampus 18 (2008) 310-316
18. Boutros N.N., Overall J., and Zouridakis G. Test-retest reliability of the P50 mid-latency auditory evoked response. Psychiatry Research 39 (1991) 181-192
19. Boutros N.N., Trautner P., Korzyukov O., Grunwald T., Burroughs S., Elger C.E., et al. Mid-latency auditory-evoked responses and sensory gating in focal epilepsy: A preliminary exploration. Journal of Neuropsychiatry and Clinical Neurosciences 18 (2006) 409-416
20. Boutros N.N., Uretsky N.J., Lui J.J., and Millana R.B. Effects of repeated cocaine administration on sensory inhibition in rats: Preliminary data. Biological Psychiatry 41 (1997) 461-466
21. Brown V.J., and Bowman E.M. Rodent models of prefrontal cortical function. Trends in Neurosciences 25 (2002) 340-343
22. Cadenhead K.S., Light G.A., Shafer K.M., and Braff D.L. P50 suppression in individuals at risk for schizophrenia: The convergence of clinical, familial, and vulnerability marker risk assessment. Biological Psychiatry 57 (2005) 1504-1509
23. Clementz B.A., Geyer M.A., and Braff D.L. Poor P50 suppression among schizophrenia patients and their first-degree biological relatives. American Journal of Psychiatry 155 (1998) 1691-1694
24. Corcoran K.A., and Quirk G.J. Activity in prelimbic cortex is necessary for the expression of learned, but not innate, fears. Journal of Neuroscience 27 (2007) 840-844
25. Cromwell H.C., Anstrom K., Azarov A., and Woodward D.J. Auditory inhibitory gating in the amygdala: Single-unit analysis in the behaving rat. Brain Research 1043 (2005) 12-23
26. Cromwell H.C., Klein A., and Mears R.P. Single unit and population responses during inhibitory gating of striatal activity in freely moving rats. Neuroscience 146 (2007) 69-85
27. Cromwell H.C., Mears R.P., Wan L., and Boutros N.N. Sensory gating: A translational effort from basic to clinical science. Clinical EEG and Neuroscience 39 (2008) 69-72
28. Cullum C.M., Harris J.G., Waldo M.C., Smernoff E., Madison A., Nagamoto H., et al. Neurophysiological and neuropsychological evidence for attentional dysfunction in schizophrenia. Schizophrenia Research 10 (1993) 131-141
29. Dalley J.W., Cardinal R.N., and Robbins T.W. Prefrontal executive and cognitive functions in rodents: Neural and neurochemical substrates. Neuroscience and Biobehavioral Reviews 28 (2004) 771-784
30. Eccles J.C. The inhibitory pathways of the central nervous system (1969), Thomas, Springfield, MA
31. Feenstra M.G., Vogel M., Botterblom M.H., Joosten R.N., and de Bruin J.P. Dopamine and noradrenaline efflux in the rat prefrontal cortex after classical aversive conditioning to an auditory cue. European Journal of Neuroscience 13 (2001) 1051-1054
32. Finlay J.M., Zigmond M.J., and Abercrombie E.D. Increased dopamine and norepinephrine release in medial prefrontal cortex induced by acute and chronic stress: Effects of diazepam. Neuroscience 64 (1995) 619-628
33. Franks R.D., Adler L.E., Waldo M.C., Alpert J., and Freedman R. Neurophysiological studies of sensory gating in mania: Comparison with schizophrenia. Biological Psychiatry 18 (1983) 989-1005
34. Freedman R., Adler L.E., Bickford P., Byerley W., Coon H., Cullum C.M., et al. Schizophrenia and nicotinic receptors. Harvard Review of Psychiatry 2 (1994) 179-192
35. Freedman R., Adler L.E., Myles-Worsley M., Nagamoto H.T., Miller C., Kisley M., et al. Inhibitory gating of an evoked response to repeated auditory stimuli in schizophrenic and normal subjects. Human recordings, computer simulation, and an animal model. Archives of General Psychiatry 53 (1996) 1114-1121
36. Fuerst D.R., Gallinat J., and Boutros N.N. Range of sensory gating values and test-retest reliability in normal subjects. Psychophysiology 44 (2007) 620-626
37. Gallagher M., Graham P.W., and Holland P.C. The amygdala central nucleus and appetitive Pavlovian conditioning: Lesions impair one class of conditioned behavior. Journal of Neuroscience 10 (1990) 1906-1911
38. Ghisolfi E.S., Heldt E., Zanardo A.P., Strimitzer Jr. I.M., Prokopiuk A.S., Becker J., et al. P50 sensory gating in panic disorder. Journal of Psychiatric Research 40 (2006) 535-540
39. Ghisolfi E.S., Margis R., Becker J., Zanardo A.P., Strimitzer I.M., and Lara D.R. Impaired P50 sensory gating in post-traumatic stress disorder secondary to urban violence. International Journal of Psychophysiology 51 (2004) 209-214
40. Gilmartin M.R., and McEchron M.D. Single neurons in the medial prefrontal cortex of the rat exhibit tonic and phasic coding during trace fear conditioning. Behavioral Neuroscience 119 (2005) 1496-1510
41. Gottesman I.I., and Gould T.D. The endophenotype concept in psychiatry: Etymology and strategic intentions. American Journal of Psychiatry 160 (2003) 636-645
42. Grunwald T., Boutros N.N., Pezer N., von Oertzen J., Fernandez G., Schaller C., et al. Neuronal substrates of sensory gating within the human brain. Biological Psychiatry 53 (2003) 511-519
43. Hajos M. Targeting information-processing deficit in schizophrenia: A novel approach to psychotherapeutic drug discovery. Trends in Pharmacological Sciences 27 (2006) 391-398
44. Jackson M.E., and Moghaddam B. Stimulus-specific plasticity of prefrontal cortex dopamine neurotransmission. Journal of Neurochemistry 88 (2004) 1327-1334
45. Jessen F., Kucharski C., Fries T., Papassotiropoulos A., Hoenig K., Maier W., et al. Sensory gating deficit expressed by a suppression of the P50 event-related potentials in patients with Alzheimer's disease. American Journal of Psychiatry 158 (2001) 1319-1321
46. Johnson M.R., and Adler L.E. Transient impairment in P50 auditory sensory gating induced by a cold-pressor test. Biological Psychiatry 33 (1993) 380-387
47. Judd L.L., McAdams L., Budnick B., and Braff D.L. Sensory gating deficits in schizophrenia: New results. American Journal of Psychiatry 149 (1992) 488-493
48. Kisley M.A., Olincy A., and Freedman R. The effect of state on sensory gating: Comparison of waking, REM and non-REM sleep. Clinical Neurophysiology 112 (2001) 1154-1165
49. Knight R.T., Staines W.R., Swick D., and Chao L.L. Prefrontal cortex regulates inhibition and excitation in distributed neural networks. Acta Psychologica (Amsterdam) 101 (1999) 159-178
50. Korzyukov O., Pflieger M.E., Wagner M., Bowyer S.M., Rosburg T., Sundaresan K., et al. Generators of the intracranial P50 response in auditory sensory gating. NeuroImage 35 (2007) 814-826
51. Krause M., Hoffmann W.E., and Hajos M. Auditory sensory gating in hippocampus and reticular thalamic neurons in anesthetized rats. Biological Psychiatry 53 (2003) 244-253
52. Lang P.J., and Davis M. Emotion, motivation, and the brain: Reflex foundations in animal and human research. Progress in Brain Research 156 (2006) 3-29
53. Lawrie S.M., McIntosh A.M., Hall J., Owens D.G., and Johnstone E.C. Brain structure and function changes during the development of schizophrenia: The evidence from studies of subjects at increased genetic risk. Schizophrenia Bulletin 34 (2008) 330-340
54. LeDoux J. Fear and the brain: Where have we been, and where are we going?. Biological Psychiatry 44 (1998) 1229-1238
55. LeDoux J. The emotional brain, fear, and the amygdala. Cellular and Molecular Neurobiology 23 (2003) 727-738
56. Lee I., and Kesner R.P. Time-dependent relationship between the dorsal hippocampus and the prefrontal cortex in spatial memory. Journal of Neuroscience 23 (2003) 1517-1523
57. Louchart-de la Chapelle S., Levillain D., Menard J.F., Van der Elst A., Allio G., Haouzir S., et al. P50 inhibitory gating deficit is correlated with the negative symptomatology of schizophrenia. Psychiatry Research 136 (2005) 27-34
58. Marquis J.P., Killcross S., and Haddon J.E. Inactivation of the prelimbic, but not infralimbic, prefrontal cortex impairs the contextual control of response conflict in rats. European Journal of Neuroscience 25 (2007) 559-566
59. McEchron M.D., Bouwmeester H., Tseng W., Weiss C., and Disterhoft J.F. Hippocampectomy disrupts auditory trace fear conditioning and contextual fear conditioning in the rat. Hippocampus 8 (1998) 638-646
60. McLaughlin J., Skaggs H., Churchwell J., and Powell D.A. Medial prefrontal cortex and pavlovian conditioning: Trace versus delay conditioning. Behavioral Neuroscience 116 (2002) 37-47
61. Mears R.P., Klein A.C., and Cromwell H.C. Auditory inhibitory gating in medial prefrontal cortex: Single unit and local field potential analysis. Neuroscience 141 (2006) 47-65
62. Moghaddam B. Stress preferentially increases extraneuronal levels of excitatory amino acids in the prefrontal cortex: Comparison to hippocampus and basal ganglia. Journal of Neurochemistry 60 (1993) 1650-1657
63. Moghaddam B., and Homayoun H. Divergent plasticity of prefrontal cortex networks. Neuropsychopharmacology 33 (2008) 42-55
64. Moghaddam B., Roth R.H., and Bunney B.S. Characterization of dopamine release in the rat medial prefrontal cortex as assessed by in vivo microdialysis: Comparison to the striatum. Neuroscience 36 (1990) 669-676
65. Morgane P.J., Galler J.R., and Mokler D.J. A review of systems and networks of the limbic forebrain/limbic midbrain. Progress in Neurobiology 75 (2005) 143-160
66. Moxon K.A., Gerhardt G.A., Bickford P.A., Austin K., Rose G.M., Woodward D.J., et al. Mulitple single units and population responses during inhibitory gating of hippocampal auditorey response in freely-moving rats. Brain Research 825 (1999) 75-85
67. Murphy B.L., Arnsten A.F., Goldman-Rakic P.S., and Roth R.H. Increased dopamine turnover in the prefrontal cortex impairs spatial working memory performance in rats and monkeys. Proceedings of the National Academy of Sciences of the United States of America 93 (1996) 1325-1329
68. Murphy B.L., Arnsten A.F., Jentsch J.D., and Roth R.H. Dopamine and spatial working memory in rats and monkeys: Pharmacological reversal of stress-induced impairment. Journal of Neuroscience 16 (1996) 7768-7775
69. Neylan T.C., Fletcher D.J., Lenoci M., McCallin K., Weiss D.S., Schoenfeld F.B., et al. Sensory gating in chronic posttraumatic stress disorder: Reduced auditory P50 suppression in combat veterans. Biological Psychiatry 46 (1999) 1656-1664
70. O'Donnell P. Dopamine gating of forebrain neural ensembles. European Journal of Neuroscience 17 (2003) 429-435
71. Oranje B., Geyer M.A., Bocker K.B., Leon Kenemans J., and Verbaten M.N. Prepulse inhibition and P50 suppression: Commonalities and dissociations. Psychiatry Research 143 (2006) 147-158
72. Otani S. Prefrontal cortex function, quasi-physiological stimuli, and synaptic plasticity. Journal of Physiology Paris 97 (2003) 423-430
73. Patterson J.V., Jin Y., Gierczak M., Hetrick W.P., Potkin S., Bunney W.E., et al. Effects of temporal variability on P50 and the gating ratio in schizophrenia. Archives of General Psychiatry 57 (2000) 57-64
74. Paxinos G., and Watson C. The rat brain in stereotaxic coordinates. 4th ed. (1998), Academic Press, San Diego, CA
75. Pezze M.A., and Feldon J. Mesolimbic dopaminergic pathways in fear conditioning. Progress in Neurobiology 74 (2004) 301-320
76. Quirk G.J., and Beer J.S. Prefrontal involvement in the regulation of emotion: Convergence of rat and human studies. Current Opinion in Neurobiology 16 (2006) 723-727
77. Quirk G.J., Garcia R., and Gonzalez-Lima F. Prefrontal mechanisms in extinction of conditioned fear. Biological Psychiatry 60 (2006) 337-343
78. Quirk G.J., and Mueller D. Neural mechanisms of extinction learning and retrieval. Neuropsychopharmacology 33 (2008) 56-72
79. Rossi S., Bartalini S., Ulivelli M., Mantovani A., Di Muro A., Goracci A., et al. Hypofunctioning of sensory gating mechanisms in patients with obsessive-compulsive disorder. Biological Psychiatry 57 (2005) 16-20
80. Seamans J.K., and Yang C.R. The principal features and mechanisms of dopamine modulation in the prefrontal cortex. Progress in Neurobiology 74 (2004) 1-58
81. Siegel S.J., Connolly P., Liang Y., Lenox R.H., Gur R.E., Bilker W.B., et al. Effects of strain, novelty, and NMDA blockade on auditory-evoked potentials in mice. Neuropsychopharmacology 28 (2003) 675-682
82. Skinner R.D., Rasco L.M., Fitzgerald J., Karson C.N., Matthew M., Williams D.K., et al. Reduced sensory gating of the P1 potential in rape victims and combat veterans with posttraumatic stress disorder. Depression and Anxiety 9 (1999) 122-130
83. Smith D.A., Boutros N.N., and Schwarzkopf S.B. Reliability of P50 auditory event-related potential indices of sensory gating. Psychophysiology 31 (1994) 495-502
84. Stevens K.E., Fuller L.L., and Rose G.M. Dopaminergic and noradrenergic modulation of amphetamine-induced changes in auditory gating. Brain Research 555 (1991) 91-98
85. Suer C., Dolu N., and Ozesmi C. The effect of immobilization stress on sensory gating in mice. International Journal of Neuroscience 114 (2004) 55-65
86. Tregellas J.R., Davalos D.B., Rojas D.C., Waldo M.C., Gibson L., Wylie K., et al. Increased hemodynamic response in the hippocampus, thalamus and prefrontal cortex during abnormal sensory gating in schizophrenia. Schizophrenia Research 92 (2007) 262-272
87. Umbricht D., Vyssotky D., Latanov A., Nitsch R., Brambilla R., D'Adamo P., et al. Midlatency auditory event-related potentials in mice: Comparison to midlatency auditory ERPs in humans. Brain Research 1019 (2004) 189-200
88. Vertes R.P. Interactions among the medial prefrontal cortex, hippocampus and midline thalamus in emotional and cognitive processing in the rat. Neuroscience 142 (2006) 1-20
89. Vidal-Gonzalez I., Vidal-Gonzalez B., Rauch S.L., and Quirk G.J. Microstimulation reveals opposing influences of prelimbic and infralimbic cortex on the expression of conditioned fear. Learning & Memory 13 (2006) 728-733
90. 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
91. White P.M., Kanazawa A., and Yee C.M. Gender and suppression of mid-latency ERP components during stress. Psychophysiology 42 (2005) 720-725
92. White P.M., and Yee C.M. Effects of attentional and stressor manipulations on the P50 gating response. Psychophysiology 34 (1997) 703-711
93. Williams G.V., and Castner S.A. Under the curve: Critical issues for elucidating D1 receptor function in working memory. Neuroscience 139 (2006) 263-276
94. Wood S.J., Pantelis C., Velakoulis D., Yucel M., Fornito A., and McGorry P.D. Progressive changes in the development toward schizophrenia: Studies in subjects at increased symptomatic risk. Schizophrenia Bulletin 34 (2008) 322-329
95. Yee C.M., and White P.M. Experimental modification of P50 suppression. Psychophysiology 38 (2001) 531-539