Auditory Fear Conditioning Modulates Prepulse Inhibition in Socially Reared Rats and Isolation-Reared Rats

Behavioral Neuroscience

Volumn 122, Issue 1, 2008, Pages 107-118

  Li, Nanxin ^a   Ping, Junli ^a   Wu, Rongbin ^a   Wang, Chao ^a   Wu, Xihong ^a   Li, Liang ^a  

^a National Key Laboratory on Machine Perception   (China)

Author keywords

2 methyl 6 (phenylethynyl) pyridine; auditory fear conditioning; metabotropic glutamate receptor subtype 5; prepulse inhibition; social isolation

Indexed keywords

2 METHYL 6 (PHENYLETHYNYL)PYRIDINE; METABOTROPIC RECEPTOR 5; METABOTROPIC RECEPTOR ANTAGONIST;

ANIMAL EXPERIMENT; ARTICLE; COGNITION; CONTROLLED STUDY; FEAR; MALE; NEUROMODULATION; NONHUMAN; PREPULSE INHIBITION; RAT; REARING; SCHIZOPHRENIA; STARTLE REFLEX; STIMULUS RESPONSE;

ACOUSTIC STIMULATION; ANALYSIS OF VARIANCE; ANIMALS; BEHAVIOR, ANIMAL; CONDITIONING (PSYCHOLOGY); EXCITATORY AMINO ACID ANTAGONISTS; FEAR; HABITUATION, PSYCHOPHYSIOLOGIC; INHIBITION (PSYCHOLOGY); MALE; PYRIDINES; RATS; RATS, SPRAGUE-DAWLEY; SOCIAL ISOLATION; STARTLE REACTION; TIME FACTORS;

EID: 40749098910     PISSN: 07357044     EISSN: None     Source Type: Journal    
DOI: 10.1037/0735-7044.122.1.107     Document Type: Article

References (110)

1. Arakawa H. Interaction between isolation rearing and social development on exploratory behavior in male rats. Behavior processes 70 (2005) 223-234
2. Bach P., Issac M., and Slassi A. Metabotropic glutamate receptor 5 modulators and their potential therapeutic applications. Expert Opinion on Therapeutic Patents 17 (2007) 371-384
3. Bakshi V.P., Swerdlow N.R., Braff D.L., and Geyer M.A. Reversal of isolation rearing-induced deficits in prepulse inhibition by seroquel and olanzapine. Biological Psychiatry 43 (1998) 436-445
4. Bakshi V.P., Tricklebank M., Neijt H.C., Lehmann-Masten V., and Geyer M.A. Disruption of prepulse inhibition and increases in locomotor activity by competitive N-methyl-D-aspartate receptor antagonists in rats. Journal of Pharmacology and Experimental Therapy 288 (1999) 643-652
5. Barsz K., Ison J.R., Snell K.B., and Walton J.P. Behavioral and neural measures of auditory temporal acuity in aging humans and mice. Neurobiology of Aging 23 (2002) 565-578
6. Bianchi M., Fone K.F.C., Azmi N., Heidbreder C.A., Hagan J.J., and Marsden C.A. Isolation rearing induces recognition memory deficits accompanied by cytoskeletal alterations in rat hippocampus. European Journal of Neuroscience 24 (2006) 2894-2902
7. Bradley M.M., Codispoti M., and Lang P.J. A multi-process account of startle modulation during affective perception. Psychophysiology 43 (2006) 486-497
8. Braff D.L., and Geyer M.A. Sensorimotor gating and schizophrenia, human and animal model studies. Archives of General Psychiatry 47 (1990) 181-188
9. Braff D.L., Geyer M.A., and Swerdlow N.R. Human studies of prepulse inhibition of startle, normal subjects, patient groups, and pharmacological studies. Psychopharmacology 156 (2001) 234-258
10. Braff D.L., Grillon C., and Geyer M.A. Gating and habituation of the startle reflex in schizophrenic patients. Archives of General Psychiatry 49 (1992) 206-215
11. Braff D.L., Stone C., Callaway E., Geyer M.A., Glick I., and Bali L. Prestimulus effects on human startle reflex in normals and schizophrenics. Psychophysiology 15 (1978) 339-343
12. Braff D.L., Swerdlow N.R., and Geyer M.A. Symptom correlates of prepulse inhibition deficits in male schizophrenic patients. American Journal of Psychiatry 156 (1999) 596-602
13. Cadenhead K.S., Geyer M.A., and Braff D.L. Impaired startle prepulse inhibition and habituation in patients with schizotypal personality disorder. American Journal of Psychiatry 150 (1993) 1862-1867
14. Cadenhead K.S., Swerdlow N.R., Shafer K.M., Diaz M., and Braff D.L. Modulation of the startle response and startle laterality in relatives of schizophrenia patients and schizotypal personality disordered subjects, evidence of inhibitory deficits. American Journal of Psychiatry 157 (2000) 1660-1668
15. Campbell U.C., Lalwani K., Hernandez L., Kinney G.G., Conn P.J., and Bristow L.J. The mGluR5 antagonist 2-methyl-6-(phenylethynyl)-pyridine (MPEP) potentiates PCP-induced cognitive deficits in rats. Psychopharmacology 175 (2004) 310-318
16. Cilia J., Hatcher P.D., and Reavill C. Long-term evaluation of isolation-rearing induced prepulse inhibition deficits in rats, an update. Psychopharmacology 180 (2005) 57-62
17. Cilia J., Reavill C., and Hagan J.J. Long-term evaluation of isolation-rearing induced prepulse inhibition deficits in rats. Psychopharmacology 156 (2001) 327-337
18. Dalley J.W., Theobald D.E., Pereira E.A.C., Li P.M.M.C., and Robbins T.W. Specific abnormalities in serotonin release in the prefrontal cortex of isolation-reared rats measured during behavioural performance of a task assessing visuospatial attention and impulsivity. Psychopharmacology 164 (2002) 329-340
19. Dawson M.E., Schell A.M., Hazlett E.A., Nuechterlein K.H., and Filion D.L. On the clinical and cognitive meaning of impaired sensorimotor gating in schizophrenia. Psychiatry Research 96 (2000) 187-197
20. Day-Wilson K.M., Jones D.N.C., Southam E., Cilia J., and Totterdell S. Medial prefrontal cortex volume loss in rats with isolation rearing-induced deficits in prepulse inhibition of acoustic startle. Neuroscience 141 (2006) 1113-1121
21. Decker M.W., Curzon P., and Brioni J.D. Influence of separate and combined septal and amygdala lesions on memory, acoustic startle, anxiety, and locomotor activity in rats. Neurobiology of Learning and Memory 64 (1995) 156-168
22. Djouma E., Card K., Lodge D.J., and Lawrence A.J. The CRF1 receptor antagonist, antalarmin, reverses isolation-induced up-regulation of dopamine D-2 receptors in the amygdala and nucleus accumbens of Fawn-Hooded rats. European Journal of Neuroscience 23 (2006) 3319-3327
23. Doron N.N., and LeDoux J.E. Organization of projections to the lateral amygdala from auditory and visual areas of the thalamus in the rat. Journal of Comparative Neurology 412 (1999) 383-409
24. Ellenbroek B.A., and Cools A.R. The neurodevelopment hypothesis of schizophrenia, Clinical evidence and animal models. Neuroscience Research Communications 22 (1998) 127-136
25. Fendt M. Injections of the NMDA receptor antagonist aminophosphonopentanoic acid into the lateral nucleus of the amygdala block the expression of fear-potentiated startle and freezing. Journal of Neuroscience 21 (2001) 4111-4115
26. Fendt M., and Schmid S. Metabotropic glutamate receptors are involved in amygdaloid plasticity. European Journal of Neuroscience 15 (2002) 1535-1541
27. Fendt M., Schwienbacher I., and Koch M. Amygdaloid N-methyl-D-aspartate and gamma-aminobutyric acidA receptors regulate sensorimotor gating in a dopamine-dependent way in rats. Neuroscience 98 (2000) 55-60
28. Filion D.L., and Ciranni M. The function significance of prepulse inhibition, A test of the protection of processing theory. Psychophysiology 31 Suppl. (1994) S46
29. Filion D.L., Dawson M.E., and Schell A.M. Modification of the acoustic startle-reflex eyeblink, a tool for investigating early and late attentional processes. Biological Psychology 35 (1993) 185-200
30. Filion D.L., and Poje A.B. Selective and nonselective attention effects on prepulse inhibition of startle, a comparison of task and no-task protocols. Biological Psychology 64 (2003) 283-296
31. Geyer M.A., Krebs-Thomson K., Braff D.L., and Swerdlow N.R. Pharmacological studies of prepulse inhibition models of sensorimotor gating deficits in schizophrenia, a decade in review. Psychopharmacology 156 (2001) 117-154
32. 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. Biological Psychiatry 34 (1993) 361-372
33. Goosens K.A., and Maren S. Contextual and auditory fear conditioning are mediated by the lateral, basal, and central amygdaloid nuclei in rats. Learning and Memory 8 (2001) 148-155
34. Graham F.K. The more or less startling effects of weak prestimulation. Psychophysiology 12 (1975) 238-248
35. Grillon C., Ameli R., Charney D.S., Krystal J., and Braff D.L. Startle gating deficits occur across prepulse intensities in schizophrenic patients. Biological Psychiatry 32 (1992) 939-943
36. Grillon C., and Davis M. Effects of stress and shock anticipation on prepulse inhibition of the startle reflex. Psychophysiology 34 (1997) 511-517
37. Gupta D.S., McCullumsmith G.E., Beneyto M., Haroutunian V., Davis K.L., and Meador-Woodruff J.H. Metabotropic glutamate receptor protein expression in the prefrontal cortex and striatum in schizophrenia. Synapse 57 (2005) 123-131
38. Harte M.K., Powell S.B., Reynolds L.M., Swerdlow N.R., Geyer M.A., and Reynolds G.P. Reduced N-acetylaspartate in the temporal cortex of rats reared in isolation. Biological Psychiatry 56 (2004) 296-299
39. Hazlett E.A., Buchsbaum M.S., Tang C.Y., Fleischman M.B., Wei T.C., Byne W., et al. Thalamic activation during an attention-to-prepulse startle modification paradigm: A functional MRI study. Biological Psychiatry 50 (2001) 281-291
40. Hazlett E.A., Levine J., Buchsbaum M.S., Silverman J.M., New A., Sevin E.M., et al. Deficient attentional modulation of the startle response in patients with schizotypal personality disorder. American Journal of Psychiatry 160 (2003) 1621-1626
41. Heidbreder C.A., Foxton R., Cilia J., Hughes Z.A., Shah A.J., Atkins A., et al. Increased responsiveness of dopamine to atypical, but not typical antipsychotics in the medial prefrontal cortex of rats reared in isolation. Psychopharmacology 156 (2001) 338-351
42. Heidbreder C.A., Weiss I.C., Domeney A.M., Pryce C., Homber J., Hedou G., et al. Behavioral, neurochemical and endocrinological characterization of the early isolation syndrome. Neuroscience 100 (2000) 749-768
43. Hoffman H.S., and Ison J.R. Reflex modification in the domain of startle, I. Some empirical findings and their implications for how the nervous system processes sensory input. Psychological Review 87 (1980) 175-189
44. Huang J., Yang Z., Ping J., Liu X., Wu X., and Li L. The influence of the perceptual or fear learning on rats' prepulse inhibition induced by changes in the correlation between two spatially separated noise sounds. Hearing Research 223 (2007) 1-10
45. Ison J.R., Agrawal P., Pak J., and Vaughn W.J. Changes in temporal acuity with age and with hearing impairment in the mouse: A study of the acoustic startle reflex and its inhibition by brief decrements in noise level. Journal of the Acoustical Society of America 104 (1998) 1696-1704
46. Ison J.R., and Bowen G.P. Scopolamine reduces sensitivity to auditory gaps in the rat, suggesting a cholinergic contribution to temporal acuity. Hearing Research 145 (2000) 169-176
47. Ison J.R., and Hoffman H.S. Reflex modification in the domain of startle, II. The anomalous history of a robust and ubiquitous phenomenon. Psychological Review 94 (1983) 3-17
48. Jennings P.D., Schell A.M., Filion D.L., and Dawson M.E. Tracking early and late stages of information processing, contributions of startle eyeblink reflex modification. Psychophysiology 33 (1996) 148-155
49. Jones G.H., Hernandez T.D., and Kendall D.A. Dopaminergic and serotonergic function following isolation rearing in rats-study of behavioral-response and postmortem and invivo neurochemistry. Pharmacology Biochemistry and Behavior 43 (1992) 17-35
50. Jones G.H., Marsden C.A., and Robbins T.W. Behavioural rigidity and rule-learning deficits following isolation-rearing in the rat, neurochemical correlates. Behavioural Brain Research 43 (1991) 35-50
51. Karper L.P., Freeman G.K., Grillon C., Morgan C.A., Charney D.S., and Krystal H.J. Preliminary evidence of an association between sensorimotor gating and distractibility in psychosis. Journal of Neuropsychiatritry and Clinical Neuroscience 8 (1996) 60-66
52. Kedzior K.K., and Martin-Iverson M.T. Attention-dependent reduction in prepulse inhibition of the startle reflex in cannabis users and schizophrenia patients - A pilot study. European Journal of Pharmacology 560 (2007) 176-182
53. Koros E., Rosenbrock H., Birk G., Weiss C., and Sams-Dodd F. The selective mGlu5 receptor antagonist MTEP, similar to NMDA receptor antagonists, induces social isolation in rats. Neuropsychopharmacology 32 (2007) 562-576
54. Kumari V., Soni W., Mathew V.M., and Sharma T. Prepulse inhibition of the startle response in men with schizophrenia, Effects of age of onset of illness, symptoms, and medication. Archives of General Psychiatry 57 (2000) 609-614
55. Kumari V., Soni W., and Sharma T. Normalization of information processing deficits in schizophrenia with clozapine. American Journal of Psychiatry 156 (1999) 1046-1051
56. Landis C., and Hunt A. The startle pattern (1939), Farrar and Rinehart, New York
57. Lapiz M.D.S., Mateo Y., Parker T., and Marsden C. Effects of noradrenaline depletion in the brain on response to novelty in isolation-reared rats. Psychopharmacology 152 (2000) 312-320
58. LeDoux J.E., Farb C., and Ruggiero D.A. Topographic organization of neurons in the acoustic thalamus that project to the amygdala. Journal of Neuroscience 10 (1990) 1043-1054
59. Lee O.K., Lee C.J., and Choi S. Induction mechanisms for L-LTP at thalamic input synapses to the lateral amygdala, requirement of mGluR5 activation. Neuroreport 13 (2002) 685-691
60. Leitner D.S., and Girten E.M. Dopamine receptor agonists alter gap prestimulus modulation. Psychopharmacology 134 (1997) 213-220
61. Li L., and Shao F. Impaired auditory sensorimotor gating: An animal model of schizophrenia. Chinese Science Bulletin 48 (2003) 2031-2037
62. Li L., and Yue Q. Auditory gating processes and binaural inhibition in the inferior colliculus. Hearing Research 168 (2002) 113-124
63. Li N., Wu X., and Li L. Chronic administration of clozapine alleviates reversal-learning impairment in isolation-reared rats. Behavioural Pharmacology 18 (2007) 135-145
64. Maren S. Synaptic transmission and plasticity in the amygdala - An emerging physiology of fear conditioning circuits. Molecular Neurobiology 13 (1996) 1-22
65. Maren S., Yap S.A., and Goosens K.A. The amygdala is essential for the development of neuronal plasticity in the medial geniculate nucleus during auditory fear conditioning in rats. Journal of Neuroscience 21 (2001) RC135
66. Marenco S., and Weinberger D.R. The neurodevelopmental hypothesis of schizophrenia: Following a trail of evidence from cradle to grave. Developmental Psychopathology 12 (2000) 501-527
67. McGrath J.J., Feron F.P., Burne T.H.J., Mackay-Sim A., and Eyles D.W. The neurodevelopmental hypothesis of schizophrenia: A review of recent developments. Annals of Medicine 35 (2003) 86-93
68. Melendez R.I., Gregory M.L., Bardo M.T., and Kalivas P.W. Impoverished rearing environment alters metabotrophic glutamate receptor expression and function in the prefrontal cortex. Neuropsychopharmacology 29 (2004) 1980-1987
69. Meyer U., Feldon J., Schedlowskib M., and Yee B.K. Towards an immuno-precipitated neurodevelopmental animal model of schizophrenia. Neuroscience and Biobehavioral Review 29 (2005) 913-947
70. Muchimapura S., Fulford A.J., Mason R., and Marsden C.A. Isolation rearing in the rat disrupts the hippocampal response to stress. Neuroscience 112 (2002) 697-705
71. Muchimapura S., Mason R., and Marsden C.A. Effect of isolation rearing on pre- and post-synaptic serotonergic function in the rat dorsal hippocampus. Synapse 47 (2003) 209-217
72. Mussat-Whitlow B.J., and Blumenthal T.D. Impact of acoustic and vibrotactile prepulse on acoustic and electrical blink reflexes, startle inhibition and task accuracy results. Psychophysiology 34 Suppl. (1997) S66
73. Norris C.M., and Blumenthal T.D. Evidence for the protection of preattentive processing during inhibition of the acoustic startle response. Psychophysiology 32 Suppl. (1995) 57
74. Norris C.M., and Blumenthal T.D. A relationship between inhibition of the acoustic startle response and the protection of prepulse processing. Psychobiology 24 (1996) 160-168
75. Parwani A., Duncan E.J., Bartlett E., Madonick S.H., Efferen T.R., Rajan R., et al. Impaired prepulse inhibition of acoustic startle in schizophrenia. Biological Psychiatry 47 (2000) 662-669
76. Paulus M.P., Bakshi V.P., and Geyer M.A. Isolation rearing affects sequential organization of motor behavior in post-pubertal but not pre-pubertal Lister and Sprague-Dawley rats. Behavioural Brain Research 94 (1998) 271-280
77. Perlstein W.M., Fiorito E., Simon R.F., and Graham F.K. Pre-stimulation effects on reflex blink and evoked potentials in normal and schizotypal subjects. Psychophysiology (Suppl.) 26 (1989) S48
78. Perlstein W.M., Fiorito E., Simon R.F., and Graham F.K. Lead stimulation effects on reflex blink, exogenous brain potentials, and loudness judgments. Psychophysiology 30 (1993) 347-358
79. Perry W., and Braff D.L. Information-processing deficits and thought-disorder in schizophrenia. American Journal of Psychiatry 151 (1994) 363-367
80. Pietraszek M., Nagel J., Gravius A., Schaefer D., and Danysz W. The role of group I metabotropic glutamate receptors in schizophrenia. Amino Acid 32 (2007) 173-178
81. Poremba A., and Gabriel M. Amygdalar efferents initiate auditory thalamic discriminative training-induced neuronal activity. Journal of Neuroscience 21 (2001) 270-278
82. Preece M.A., Dalley J.W., and Theobald D.H. Region specific changes in forebrain 5-hydroxytryptamine(1A) and 5-hydroxytryptamine(2A) receptors in isolation-reared rats, An in vitro autoradiography study. Neuroscience 123 (2004) 725-732
83. Reboucas R., and Schimidek W.R. Handing and isolation in three strains of rats affect open field, exploration, hoarding and predation. Physiology and Behavior 62 (1997) 1159-1164
84. Rehn A.E., and Rees S.M. Investigating the neurodevelopmental hypothesis of schizophrenia. Clinical Experimental Pharmacology and Physiology 32 (2005) 687-696
85. Riedel G., Casabona G., Platt B., Macphail E.M., and Nicoletti F. Fear conditioning-induced time- and subregion-specific increase in expression of mGlu5 receptor protein in rat hippocampus. Neuropharmacology 39 (2000) 1943-1951
86. Rodrigues S.M., Bauer E.P., Farb C.R., Schafe G.E., and LeDoux J.E. The group I metabotropic glutamate receptor mGluR5 is required for fear memory formation and long-term potentiation in the lateral amygdala. Journal of Neuroscience 22 (2002) 5219-5229
87. Romanski L.M., and LeDoux J.E. Equipotentiality of thalamoamygdala and thalamocorticoamygdala circuits in auditory fear conditioning. Journal of Neuroscience 12 (1992) 4501-4509
88. Romanski L.M., and LeDoux J.E. Information cascade from primary auditory-cortex to the amygdala-corticocortical and corticoamygdaloid projections of temporal cortex in the rat. Cerebral Cortex 3 (1993) 515-532
89. Schell A.M., Dawson M.E., Hazlett E.A., and Filion D.L. Attentional modulation of startle in psychosis-prone college students. Psychophysiology 32 (1995) 266-273
90. Schell A.M., Wynn J.K., Dawson M.E., Sinaii N., and Niebala C.B. Automatic and controlled attentional processes in startle eyeblink modification, Effects of habituation of the prepulse. Psychophysiology 37 (2000) 409-417
91. Schulz B., Fendt M., Gasparini F., Lingenhohl K., Kuhn R., and Koch M. The metabotropic glutamate receptor antagonist 2-methyl-6-(phenylethynyl)-pyridine (MPEP) blocks fear conditioning in rats. Neuropharmacology 41 (2001) 1-7
92. Sikes R.W., and Vogt B.A. Nociceptive neurons in area 24 of rabbit cingulate cortex. Journal of Neurophysiology 68 (1992) 1720-1732
93. Simonyi A., Schachtman T.R., and Christoffersen G.R.J. The role of metabotropic glutamate receptor 5 in learning and memory processes. Drug News and Perspectives 18 (2005) 353-361
94. Stevenson C.W., and Gratton A. Role of basolateral amygdala dopamine in modulating prepulse inhibition and latent inhibition in the rat. Psychopharmacology 176 (2004) 139-145
95. Swerdlow N.R., Geyer M.A., and Braff D.L. Neural circuit regulation of prepulse inhibition of startle in the rat, current knowledge and future challenges. Psychopharmacology 156 (2001) 194-215
96. Thornea G.L., Dawsona M.E., and Schell A.M. Attention and prepulse inhibition, the effects of task-relevant, irrelevant, and no-task conditions. International Journal of Psychophysiology 56 (2005) 121-128
97. van den Buuse M., Garner B., Gogos A., and Kusljic S. Importance of animal models in schizophrenia research. Australia and New Zealand Journal of Psychiatry 39 (2005) 550-557
98. van den Buuse M., Garner B., and Koch M. Neurodevelopmental animal models of schizophrenia, Effects on prepulse inhibition. Current Molecular Medicine 3 (2003) 459-471
99. Varty G.B., and Geyer M.A. Effects of isolation rearing on startle reactivity, habituation, and prepulse inhibition in male Lewis, Sprague-Dawley, and Fischer F344 rats. Behavioral Neuroscience 112 (1998) 1450-1457
100. Varty G.B., Paulus M.P., Braff D.L., and Geyer M.A. Environmental enrichment and isolation rearing in the rat, effects on locomotor behavior and startle response plasticity. Biological Psychiatry 47 (2000) 864-873
101. Villanueva L., Bing Z., Bouhassira D., and Le Bars D. Encoding of electrical, thermal, and mechanical noxious stimuli by subnucleus reticularis dorsalis neurons in the rat medulla. Journal of Neurophysiology 61 (1989) 391-402
102. Wan F.J., and Swerdlow N.R. The basolateral amygdala regulates sensorimotor gating of acoustic startle in the rat. Neuroscience 76 (1997) 715-724
103. Weinberger D.R. On the plausibility of '"The neurodevelopmental hypothesis'" of schizophrenia. Neuropsychopharmacology 14 Suppl. (1996) S1-S11
104. Weiss I.C., Domeney A.M., Moreau J., Russig H., and Feldon J. Dissociation between the effects of pre-weaning and/or post-weaning social isolation on prepulse inhibition and latent inhibition in adult Sprague-Dawley rats. Behavioural Brain Research 121 (2001) 207-218
105. Weiss I.C., and Feldon J. Environmental animal models for sensorimotor gating deficiencies in schizophrenia, a review. Psychopharmacology 156 (2001) 305-326
106. Whitaker-Azmitia P., Zhou F., Hobin J., and Borella A. Isolation-fearing of rats produces deficits as adults in the serotonergic innervation of hippocampus. Peptides 21 (2000) 1755-1759
107. Wilkinson L.S., Killcross S.S., Humby T., Hall F.S., Geyer M.A., and Robbins T.W. Social-isolation in the rat produces developmentally specidic dedicits in prepulse inhibition of the acoustic startle response without disturbing latent inhibition. Neuropsychopharmacology 10 (1994) 61-72
108. Woodson W., Farb C.R., and LeDoux J.E. Afferents from the auditory thalamus synapse on inhibitory interneurons in the lateral nucleus of the amygdala. Synapse 38 (2000) 124-137
109. Zhang J.H., Engel J.A., Ericson M., and Svensson L. Involvement of the medial geniculate body in prepulse inhibition of acoustic startle. Psychopharmacology 141 (1999) 189-196
110. Zou D., Huang J., Wu X., and Li L. Metabotropic glutamate subtype 5 receptors modulate fear-conditioning induced enhancement of prepulse inhibition in rats. Neuropharmacology 52 (2007) 476-486