Prepulse inhibition deficits in GAD65 knockout mice and the effect of antipsychotic treatment

Neuropsychopharmacology

Volumn 29, Issue 9, 2004, Pages 1610-1619

  Heldt, Scott A ^a,b   Green, Amanda ^a   Ressler, Kerry J ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b EMORY UNIVERSITY   (United States)

Author keywords

Clozapine; GAD; Glutamic acid decarboxylase; Habituation; PPI; Startle

Indexed keywords

CLOZAPINE; GLUTAMATE DECARBOXYLASE; NEUROLEPTIC AGENT;

ARTICLE; CONTROLLED STUDY; GABAERGIC SYSTEM; HABITUATION; HETEROZYGOSITY; KNOCKOUT MOUSE; MOUSE; NEUROTRANSMISSION; NONHUMAN; PREPULSE INHIBITION; PRIORITY JOURNAL; SCHIZOPHRENIA; SENSORIMOTOR CORTEX; STARTLE REFLEX; WILD TYPE;

ACOUSTIC STIMULATION; ANIMALS; ANTIPSYCHOTIC AGENTS; CLOZAPINE; DNA PRIMERS; GAMMA-AMINOBUTYRIC ACID; GENE DELETION; GENOTYPE; GLUTAMATE DECARBOXYLASE; HABITUATION, PSYCHOPHYSIOLOGIC; IN SITU HYBRIDIZATION; ISOENZYMES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; STARTLE REACTION; SYNAPTIC TRANSMISSION;

EID: 4344614806     PISSN: 0893133X     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.npp.1300468     Document Type: Article

References (80)

1. Akbarian S, Kim JJ, Potkin SG, Hagman JO, Tafazzoli A, Bunney Jr WE (1995). Gene expression for glutamic acid decarboxylase is reduced without loss of neurons in prefrontal cortex of schizophrenics. Arch Gen Psychiatry 52: 258-266.
2. Andersen MP, Pouzet B (2001). Effects of acute versus chronic treatment with typical or atypical antipsychotics on D-amphetamine-induced sensorimotor gating deficits in rats. Psychopharmacology (Berl) 156: 291-304.
3. Asada H, Kawamura Y, Maruyama K, Kume H, Ding R, Ji FY et al (1996). Mice lacking the 65kDa isoform of glutamic acid decarboxylase (GAD65) maintain normal levels of GAD67 and GABA in their brains but are susceptible to seizures. Biochem Biophys Res Commun 229: 891-895.
4. Asada H, Kawamura Y, Maruyama K, Kume H, Ding RG, Kanbara N et al (1997). Cleft palate and decreased brain gamma-aminobutyric acid in mice lacking the 67-kDa isoform of glutamic acid decarboxylase. Proc Natl Acad Sci USA 94: 6496-6499.
5. Bakshi VP, Geyer MA (1995). Antagonism of phencyclidine-induced deficits in prepulse inhibition by the putative atypical antipsychotic olanzapine. Psychopharmacology (Berl) 122: 198-201.
6. Bakshi VP, Geyer MA (1999). Ontogeny of isolation rearing-induced deficits in sensorimotor gating in rats. Physiol Behav 67: 385-392.
7. Bast T, Feldon J (2003). Hippocampal modulation of sensorimotor processes. Prog Neurobiol 70: 319-345.
8. Bast T, Zhang WN, Feldon J (2001). Hyperactivity, decreased startle reactivity, and disrupted prepulse inhibition following disinhibition of the rat ventral hippocampus by the GABA(A) receptor antagonist picrotoxin. Psychopharmacology (Berl) 156: 225-233.
9. Beasley CL, Zhang ZJ, Patten I, Reynolds GP (2002). Selective deficits in prefrontal cortical GABAergic neurons in schizophrenia defined by the presence of calcium-binding proteins. Biol Psychiatry 52: 708-715.
10. Benes FM, Berretta S (2000). Amygdalo-entorhinal inputs to the hippocampal formation in relation to schizophrenia. Ann NY Acad Sci 911: 293-304.
11. Benes FM, McSparren J, Bird ED, SanGiovanni JP, Vincent SL (1991). Deficits in small interneurons in prefrontal and cingulate cortices of schizophrenic and schizoaffective patients. Arch Gen Psychiatry 48: 996-1001.
12. Berretta S, Munno DW, Benes FM (2001). Amygdalar activation alters the hippocampal GABA system: 'partial' modelling for postmortem changes in schizophrenia. J Comp Neurol 431: 129-138.
13. Bolino F, Manna V, Di Cicco L, Di Michele V, Daneluzzo E, Rossi A et al (1992). Startle reflex habituation in functional psychoses: a controlled study. Neurosci Lett 145: 126-128.
14. Braff D, Stone C, Callaway E, Geyer M, Glick I, Bali L (1978). Prestimulus effects on human startle reflex in normals and schizophrenics. Psychophysiology 15: 339-343.
15. Braff DL, Geyer MA, Swerdlow NR (2001). Human studies of prepulse inhibition of startle: normal subjects, patient groups, and pharmacological studies. Psychopharmacology (Berl) 156: 234-258.
16. Braff DL, Grillon C, Geyer MA (1992). Gating and habituation of the startle reflex in schizophrenic patients. Arch Gen Psychiatry 49: 206-215.
17. Brody SA, Conquet F, Geyer MA (2004). Effect of antipsychotic treatment on the prepulse inhibition deficit of mGluR5 knockout mice. Psychopharmacology (Berl) 172: 187-195.
18. Caldji C, Francis D, Sharma S, Plotsky PM, Meaney MJ (2000). The effects of early rearing environment on the development of GABAA and central benzodiazepine receptor levels and novelty-induced fearfulness in the rat. Neuropsychopharmacology 22: 219-229.
19. Caldji C, Tannenbaum B, Sharma S, Francis D, Plotsky PM, Meaney MJ (1998). Maternal care during infancy regulates the development of neural systems mediating the expression of fearfulness in the rat. Proc Natl Acad Sci USA 95: 5335-5340.
20. Choi S-Y, Morales B, Lee H-K, Kirkwood A (2002). Absence of long-term depression in the visual cortex of glutamic acid decarboxylase-65 knock-out mice. J Neurosci 22: 5271-5276.
21. Cilia J, Reavill C, Hagan JJ, Jones DN (2001). Long-term evaluation of isolation-rearing induced prepulse inhibition deficits in rats. Psychopharmacology (Berl) 156: 327-337.
22. Csernansky JG, Mellentin J, Beauclair L, Lombrozo L (1988). Mesolimbic dopaminergic supersensitivity following electrical kindling of the amygdala. Biol Psychiatry 23: 285-294.
23. Davis M (1984). The mamalian startle response. In Eaton RC (ed) Neural Mechanisms of Startle Behavior. Plenum Publishing: New York, pp 287-351.
24. Dirks A, Groenink L, Westphal KG, Olivier JD, Verdouw PM, van der Gugten J et al (2003). Reversal of startle gating deficits in transgenic mice overexpressing corticotropin-releasing factor by antipsychotic drugs. Neuropsychopharmacology 28: 1790-1798.
25. Ellenbroek BA, van den Kroonenberg PT, Cools AR (1998). The effects of an early stressful life event on sensorimotor gating in adult rats. Schizophr Res 30: 251-260.
26. Faraday MM, Grunberg NE (2000). The importance of acclimation in acoustic startle amplitude and pre-pulse inhibition testing of male and female rats*1. Pharmacol Biochem Behav 66: 375-381.
27. Feifel D, Melendez G, Shilling PD (2004). Reversal of sensorimotor gating deficits in Brattleboro rats by acute administration of clozapine and a neurotensin agonist, but not haloperidol: a potential predictive model for novel antipsychotic effects. Neuropsychopharmacology 29: 731-738.
28. Finamore TL, Port RL (2000). Developmental stress disrupts habituation but spares prepulse inhibition in young rats. Physiol Behav 69: 527-530.
29. Francis DD, Szegda K, Campbell G, Martin WD, Insel TR (2003). Epigenetic sources of behavioral differences in mice. Nat Neurosci 6: 445-446.
30. Geyer MA, Krebs-Thomson K, Braff DL, Swerdlow NR (2001). Pharmacological studies of prepulse inhibition models of sensorimotor gating deficits in schizophrenia: a decade in review. Psychopharmacology (Berl) 156: 117-154.
31. Guidotti A, Auta J, Davis JM, Di-Giorgi-Gerevini V, Dwivedi Y, Grayson DR et al (2000). Decrease in reelin and glutamic acid decarboxylase67 (GAD67) expression in schizophrenia and bipolar disorder: a postmortem brain study. Arch Gen Psychiatry 57: 1061-1069.
32. Hashimoto T, Volk DW, Eggan SM, Mirnics K, Pierri JN, Sun Z et al (2003). Gene expression deficits in a subclass of GABA neurons in the prefrontal cortex of subjects with schizophrenia. J Neurosci 23: 6315-6326.
33. Heckers S, Stone D, Walsh J, Shick J, Koul P, Benes FM (2002). Differential hippocampal expression of glutamic acid decarboxylase 65 and 67 messenger RNA in bipolar disorder and schizophrenia. Arch Gen Psychiatry 59: 521-529.
34. Impagnatiello F, Guidotti AR, Pesold C, Dwivedi Y, Caruncho H, Pisu MG et al (1998). A decrease of reelin expression as a putative vulnerability factor in schizophrenia. Proc Natl Acad Sci USA 95: 15718-15723.
35. Kalus P, Bondzio J, Federspiel A, Muller TJ, Zuschratter W (2002). Cell-type specific alterations of cortical interneurons in schizophrenic patients. Neuroreport 13: 713-717.
36. Kash SF, Johnson RS, Tecott LH, Noebels JL, Mayfield RD, Hanahan D et al (1997). Epilepsy in mice deficient in the 65-kDa isoform of glutamic acid decarboxylase. Proc Natl Acad Sci USA 94: 14060-14065.
37. Koch M, Ebert U (1998). Deficient sensorimotor gating following seizures in amygdala-kindled rats. Biol Psychiatry 44: 290-297.
38. Koch M, Schnitzler HU (1997). The acoustic startle response in rats - circuits mediating evocation, inhibition and potentiation. Behav Brain Res 89: 35-49.
39. Leaton RN, Cassella JV, Borszcz GS (1985). Short-term and long-term habituation of the acoustic startle response in chronic decerebrate rats. Behav Neurosci 99: 901-912.
40. Lehmann J, Pryce CR, Feldon J (1999). Sex differences in the acoustic startle response and prepulse inhibition in Wistar rats. Behav Brain Res 104: 113-117.
41. Le Pen G, Moreau JL (2002). Disruption of prepulse inhibition of startle reflex in a neurodevelopmental model of schizophrenia: reversal by clozapine, olanzapine and risperidone but not by haloperidol. Neuropsychopharmacology 27: 1-11.
42. Lipska BK, Lerman DN, Khaing ZZ, Weickert CS, Weinberger DR (2003). Gene expression in dopamine and GABA systems in an animal model of schizophrenia: effects of antipsychotic drugs. Eur J Neurosci 18: 391-402.
43. Lipska BK, Weinberger DR (2000). To model a psychiatric disorder in animals: schizophrenia as a reality test. Neuropsychopharmacology 23: 223-239.
44. Logue SF, Owen EH, Rasmussen DL, Wehner JM (1997). Assessment of locomotor activity, acoustic and tactile startle, and prepulse inhibition of startle in inbred mouse strains and F1 hybrids: Implications of genetic background for single gene and quantitative trait loci analyses. Neuroscience 80: 1075-1086.
45. Ludewig K, Geyer MA, Vollenweider FX (2003). Deficits in prepulse inhibition and habituation in never-medicated, first-episode schizophrenia. Biol Psychiatry 54: 121-128.
46. Martinez ZA, Oostwegel J, Geyer MA, Ellison GD, Swerdlow NR (2000). 'Early' and 'late' effects of sustained haloperidol on apomorphine- and phencyclidine-induced sensorimotor gating deficits. Neuropsychopharmacology 23: 517-527.
47. Matsumoto K, Nomura H, Murakami Y, Taki K, Takahata H, Watanabe H (2003). Long-term social isolation enhances picrotoxin seizure susceptibility in mice: up-regulatory role of endogenous brain allopregnanolone in GABAergic systems. Pharmacol Biochem Behav 75: 831-835.
48. Miner LA, Sarter M (1999). Intra-accumbens infusions of antisense oligodeoxynucleotides to one isoform of glutamic acid decarboxylase mRNA, GAD65, but not to GAD67 mRNA, impairs sustained attention performance in the rat. Brain Res Cogn Brain Res 7: 269-283.
49. Ojima K, Matsumoto K, Watanabe H (1997). Flumazenil reverses the decrease in the hypnotic activity of pentobarbital by social isolation stress: are endogenous benzodiazepine receptor ligands involved? Brain Res 745: 127-133.
50. Paylor R, Crawley JN (1997). Inbred strain differences in prepulse inhibition of the mouse startle response. Psychopharmacology (Berl) 132: 169-180.
51. Phillips AG, Ahn S, Rowland JG (2003). Amygdalar control of the mesocorticolimbic dopamine system: parallel pathways to motivated behavior. Neurosci Biobehav Rev 27: 543-554.
52. Ralph-Williams RJ, Lehmann-Masten V, Geyer MA (2003). Dopamine D1 rather than D2 receptor agonists disrupt prepulse inhibition of startle in mice. Neuropsychopharmacology 28: 108-118.
53. Rasmussen K, Gates MR, Burger JE, Czachura JF (1997). The novel atypical antipsychotic olanzapine, but not the CCK-B antagonist LY288513, blocks apomorphine-induced disruption of pre-pulse inhibition. Neurosci Lett 222: 61-64.
54. Remington G (2003). Understanding antipsychotic 'atypicality': a clinical and pharmacological moving target. J Psychiatry Neurosci 28: 275-284.
55. Ressler KJ, Paschall G, Zhou XL, Davis M (2002). Regulation of synaptic plasticity genes during consolidation of fear conditioning. J Neurosci 22: 7892-7902.
56. Russig H, Spooren W, Durkin S, Feldon J, Yee BK (2004). Apomorphine-induced disruption of prepulse inhibition that can be normalised by systemic haloperidol is insensitive to clozapine pretreatment. Psychopharmacology (Berl) (in press).
57. Serra M, Pisu MG, Littera M, Papi G, Sanna E, Tuveri F et al (2000). Social isolation-induced decreases in both the abundance of neuroactive steroids and GABA(A) receptor function in rat brain. J Neurochem 75: 732-740.
58. Sheikh SN, Martin SB, Martin DL (1999). Regional distribution and relative amounts of glutamate decarboxylase isoforms in rat and mouse brain. Neurochem Int 35: 73-80.
59. Shi L, Fatemi SH, Sidwell RW, Patterson PH (2003). Maternal influenza infection causes marked behavioral and pharmacological changes in the offspring. J Neurosci 23: 297-302.
60. Soghomonian JJ, Martin DL (1998). Two isoforms of glutamate decarboxylase: why? Trends Pharmacol Sci 19: 500-505.
61. Stork O, Ji FY, Kaneko K, Stork S, Yoshinobu Y, Moriya T et al (2000). Postnatal development of a GABA deficit and disturbance of neural functions in mice lacking GAD65. Brain Res 865: 45-58.
62. Stork O, Yamanaka H, Stork S, Kume N, Obata K (2003). Altered conditioned fear behavior in glutamate decarboxylase 65 null mutant mice. Genes Brain Behav 2: 65-70.
63. Swerdlow NR, Braff DL, Taaid N, Geyer MA (1994). Assessing the validity of an animal model of deficient sensorimotor gating in schizophrenic patients. Arch Gen Psychiatry 51: 139-154.
64. Swerdlow NR, Geyer MA (1993). Clozapine and haloperidol in an animal model of sensorimotor gating deficits in schizophrenia. Pharmacol Biochem Behav 44: 741-744.
65. Swerdlow NR, Geyer MA, Braff DL (2001). Neural circuit regulation of prepulse inhibition of startle in the rat: current knowledge and future challenges. Psychopharmacology (Berl) 156: 194-215.
66. Swerdlow NR, Platten A, Hanlon FM, Martinez ZA, Printz MP, Auerbach P (2003). Sensitivity to sensorimotor gating-disruptive effects of apomorphine in two outbred parental rat strains and their F1 and N2 progeny. Neuropsychopharmacology 28: 226-234.
67. Erdlow NR, Geyer MA (1993). Clozapine and haloperidol in an animal model of sensorimotor gating deficits in schizophrenia. Pharmacology, Biochemistry and Behavior 44: 741-744.
68. Todtenkopf MS, Benes FM (1998). Distribution of glutamate decarboxylase65 immunoreactive puncta on pyramidal and nonpyramidal neurons in hippocampus of schizophrenic brain. Synapse 29: 323-332.
69. Varty GB, Higgins GA (1995). Examination of drug-induced and isolation-induced disruptions of prepulse inhibition as models to screen antipsychotic drugs. Psychopharmacology (Berl) 122: 15-26.
70. Volk DW, Lewis DA (2002). Impaired prefrontal inhibition in schizophrenia: relevance for cognitive dysfunction. Physiol Behav 77: 501-505.
71. Wan FJ, Taaid N, Swerdlow NR (1996). Do D1/D2 interactions regulate prepulse inhibition in rats? Neuropsychopharmacology 14: 265-274.
72. Wang JH, Short J, Ledent C, Lawrence AJ, Buuse M (2003). Reduced startle habituation and prepulse inhibition in mice lacking the adenosine A2A receptor. Behav Brain Res 143: 201-207.
73. Weber M, Schnitzler HU, Schmid S (2002). Synaptic plasticity in the acoustic startle pathway: the neuronal basis for short-term habituation? Eur J Neurosci 16: 1325-1332.
74. Weinberger DR (1987). Implications of normal brain development for the pathogenesis of schizophrenia. Arch Gen Psychiatry 44: 660-669.
75. Westerink BH, Kwint HF, deVries JB (1996). The pharmacology of mesolimbic dopamine neurons: a dual-probe microdialysis study in the ventral tegmental area and nucleus accumbens of the rat brain. J Neurosci 16: 2605-2611.
76. Willott JF, Tanner L, O'Steen J, Johnson KR, Bogue MA, Gagnon L (2003). Acoustic startle and prepulse inhibition in 40 inbred strains of mice. Behav Neurosci 117: 716-727.
77. Yamada S, Harano M, Annoh N, Nakamura K, Tanaka M (1999). Involvement of serotonin 2A receptors in phencyclidine-induced disruption of prepulse inhibition of the acoustic startle in rats. Biol Psychiatry 46: 832-838.
78. Yu J, Kallstrom L, Wiesel FA, Johnson AE (1999). Neurochemical changes in the entopeduncular nucleus and increased oral behavior in rats treated subchronically with clozapine or haloperidol. Synapse 34: 192-207.
79. Zarate JM, Boksa P, Baptista T, Joober R (2004). Effects of clozapine on behavioral and metabolic traits relevant for schizophrenia in two mouse strains. Psychopharmacology (Berl) 171: 162-172.
80. Zhang W, Pouzet B, Jongen-Relo AL, Weiner I, Feldon J (1999). Disruption of prepulse inhibition following N-methyl-D-aspartate infusion into the ventral hippocampus is antagonized by clozapine but not by haloperidol: a possible model for the screening of atypical antipsychotics. Neuroreport 10: 2533-2538.