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Psychopharmacology

, 206:677 | Cite as

Are DBA/2 mice associated with schizophrenia-like endophenotypes? A behavioural contrast with C57BL/6 mice

  • Philipp Singer
  • Joram Feldon
  • Benjamin K. YeeEmail author
Original Investigation

Abstract

Rationale

Due to its intrinsic deficiency in prepulse inhibition (PPI), the inbred DBA/2 mouse strain has been considered as an animal model for evaluating antipsychotic drugs. However, the PPI impairment observed in DBA/2 mice relative to the common C57BL/6 strain is confounded by a concomitant reduction in baseline startle reactivity. In this study, we examined the robustness of the PPI deficit when this confound is fully taken into account.

Materials and methods

Male DBA/2 and C57BL/6 mice were compared in a PPI experiment using multiple pulse stimulus intensities, allowing the possible matching of startle reactivity prior to examination of PPI. The known PPI-enhancing effect of the antipsychotic, clozapine, was then evaluated in half of the animals, whilst the other half was subjected to two additional schizophrenia-relevant behavioural tests: latent inhibition (LI) and locomotor reaction to the psychostimulants—amphetamine and phencyclidine.

Results

PPI deficiency in DBA/2 relative to C57BL/6 mice was essentially independent of the strain difference in baseline startle reactivity. Yet, there was no evidence that DBA/2 mice were superior in detecting the PPI-facilitating effect of clozapine when startle difference was balanced. Compared with C57BL/6 mice, DBA/2 mice also showed impaired LI and a different temporal profile in their responses to amphetamine and phencyclidine.

Conclusion

Relative to the C57BL/6 strain, DBA/2 mice displayed multiple behavioural traits relevant to schizophrenia psycho- and physiopathology, indicative of both dopaminergic and glutamatergic/N-methyl-d-aspartic acid receptor dysfunctions. Further examination of their underlying neurobiological differences is therefore warranted in order to enhance the power of this specific inter-strain comparison as a model of schizophrenia.

Keywords

Amphetamine Behavioural genetic Latent inhibition Mouse Phencyclidine Prepulse inhibition Schizophrenia 

Notes

Acknowledgments

The present study was supported by the Federal Institute of Technology Zurich and the National Centre of Competence in Research (NCCR): Neural Plasticity and Repair funded by the Swiss National Science Foundation.

References

  1. Alexander RC, Wright R, Freed W (1996) Quantitative trait loci contributing to phencyclidine-induced and amphetamine-induced locomotor behavior in inbred mice. Neuropsychopharmacology 15:484–490PubMedCrossRefGoogle Scholar
  2. Ammassari-Teule M, Passino E, Restivo L, de Marsanich B (2000a) Fear conditioning in C57BL/6 and DBA/2: variability in nucleus accumbens according to the strain predisposition to show contextual- or cue-based responding. Eur J Neurosci 12:4467–4474PubMedGoogle Scholar
  3. Ammassari-Teule M, Restivo L, Passino E (2000b) Contextual-dependent effects of nucleus accumbens lesions on spatial learning in mice. Neuroreport 11:2485–2490PubMedCrossRefGoogle Scholar
  4. Ammassari-Teule M, Tozzi A, Rossi-Arnaud C, Save E, Thinus-Blanc C (1995) Reactions to spatial and nonspatial change in two inbred strains of mice: further evidence supporting the hippocampal dysfunction hypothesis in the DBA/2 strain. Psychobiology 23:284–289Google Scholar
  5. Arguello PA, Gogos JA (2006) Modeling madness in mice: one piece at a time. Neuron 52:179–196PubMedCrossRefGoogle Scholar
  6. Badiani A, Cabib S, Puglisi-Allegra S (1992) Chronic stress induces strain-dependent sensitization to the behavioral effects of amphetamine in the mouse. Pharmacol Biochem Behav 43:53–60PubMedCrossRefGoogle Scholar
  7. Baarendse PJ, van Grootheest G, Jansen RF, Pieneman AW, Ogren SO, Verhage M, Stiedl O (2008) Differential involvement of the dorsal hippocampus in passive avoidance in C57bl/6J and DBA/2J mice. Hippocampus 18:11–19PubMedCrossRefGoogle Scholar
  8. Barber RP, Vaughn JE, Wimer RE, Wimer CC (1974) Genetically-associated variations in the distribution of dentate granule cells synapses upon the pyramidal cell dendrites in the mouse hippocampus. J Comp Neurol 156:417–434PubMedCrossRefGoogle Scholar
  9. Baruch I, Hemsley D, Gray JA (1988) Differential performance of acute and chronic schizophrenic in a latent inhibition task. J Nerv Ment Dis 176:598–606PubMedCrossRefGoogle Scholar
  10. Bortolato M, Frau R, Orrù M, Piras AP, Fà M, Tuveri A, Puligheddu M, Gessa GL, Castelli MP, Mereu G, Marrosu F (2007) Activation of GABA(B) receptors reverses spontaneous gating deficits in juvenile DBA/2J mice. Psychopharmacology 194:361–369PubMedCrossRefGoogle Scholar
  11. Boulay D, Pichat P, Dargazanli G, Estenne-Bouhtou G, Terranova JP, Rogacki N, Stemmelin J, Coste A, Lanneau C, Desvignes C, Cohen C, Alonso R, Vigé X, Biton B, Steinberg R, Sevrin M, Oury-Donat F, George P, Bergis O, Griebel G, Avenet P, Scatton B (2008) Characterization of SSR103800, a selective inhibitor of the glycine transporter-1 in models predictive of therapeutic activity in schizophrenia. Pharmacol Biochem Behav 91:47–58PubMedCrossRefGoogle Scholar
  12. Bovet D, Bovet-Nitti F, Oliverio A (1969) Genetic aspects of learning and memory in mice. Science 163:139–149PubMedCrossRefGoogle Scholar
  13. Braff DL, Geyer MA, Swerdlow NR (2001) Human studies of prepulse inhibition of startle: normal subjects, patient groups, and pharmacological studies. Psychopharmacology (Berl) 156:234–258CrossRefGoogle Scholar
  14. Braff DL, Grillon C, Geyer MA (1992) Gating and habituation of the startle reflex in schizophrenic patients. Arch Gen Psychiatry 49:206–215PubMedGoogle Scholar
  15. Browman KE, Komater VA, Curzon P, Rueter LE, Hancock AA, Decker MW, Fox GB (2004) Enhancement of prepulse inhibition of startle in mice by the H3 receptor antagonists thioperamide and ciproxifan. Behav Brain Res 153:69–76PubMedCrossRefGoogle Scholar
  16. Bullock AE, Slobe BS, Vazques V, Collins AC (1997) Inbred mouse strains differ in the regulation of startle and prepulse inhibition of the startle response. Behav Neurosci 111:1353–1360PubMedCrossRefGoogle Scholar
  17. Cabib S, Bonaventura N (1997) Parallel strain-dependent susceptibility to environmentally-induced stereotypies and stress-induced behavioral sensitization in mice. Physiol Behav 61:499–506PubMedCrossRefGoogle Scholar
  18. Cabib S, Orsini C, Le Moal M, Piazza PV (2000) Abolition and reversal of strain differences in behavioral responses to drugs of abuse after a brief experience. Science 289:463–465PubMedCrossRefGoogle Scholar
  19. Coyle JT (2006) Glutamate and schizophrenia: beyond the dopamine hypothesis. Cell Mol Neurobiol 26:365–384PubMedCrossRefGoogle Scholar
  20. Cabib S, Puglisi-Allegra S, Ventura R (2002) The contribution of comparative studies in inbred strains of mice to the understanding of the hyperactive phenotype. Behav Brain Res 130:103–109PubMedCrossRefGoogle Scholar
  21. Carlsson A (1988) The current status of the dopamine hypothesis of schizophrenia. Neuropsychopharmacology 1:179–186PubMedCrossRefGoogle Scholar
  22. Carran AB, Yeudall LT, Royce JR (1964) Voltage level and skin resistance in avoidance conditioning in inbred strains of mice. J Comp Physiol Psychol 58:427–430PubMedCrossRefGoogle Scholar
  23. Chang T, Meyer U, Feldon J, Yee BK (2007) Disruption of the US pre-exposure effect and latent inhibition in two-way active avoidance by systemic amphetamine in C57BL/6 mice. Psychopharmacology (Berl) 191:211–221CrossRefGoogle Scholar
  24. Crawley JN, Belknap JK, Collins A, Crabbe JC, Frankel W, Henderson N, Hitzemann RJ, Maxson SC, Miner LL, Silva AJ, Wehner JM, Wynshaw-Boris A, Paylor R (1997) Behavioral phenotypes of inbred mouse strains: implications and recommendations for molecular studies. Psychopharmacology (Berl) 132:107–124CrossRefGoogle Scholar
  25. Csomor PA, Yee BK, Quednow BB, Stadler RR, Feldon J, Vollenweider FX (2006) The monotonic dependency of prepulse inhibition of the acoustic startle reflex on the intensity of the startle-eliciting stimulus. Behav Brain Res 174:143–150PubMedCrossRefGoogle Scholar
  26. Csomor PA, Yee BK, Feldon J, Theodoridou A, Studerus E, Vollenweider FX (2009) Impaired prepulse inhibition and prepulse-elicited reactivity but intact reflex circuit excitability in unmedicated schizophrenia patients: a comparison with healthy subjects and medicated schizophrenia patients. Schizophr Bull 35:244–255PubMedCrossRefGoogle Scholar
  27. Csomor PA, Yee BK, Vollenweider FX, Feldon J, Nicolet T, Quednow BB (2008) On the influence of baseline startle reactivity on the indexation of prepulse inhibition. Behav Neurosci 122:885–900PubMedCrossRefGoogle Scholar
  28. Depoortère R, Dargazanli G, Estenne-Bouhtou G, Coste A, Lanneau C, Desvignes C, Poncelet M, Heaulme M, Santucci V, Decobert M, Cudennec A, Voltz C, Boulay D, Terranova JP, Stemmelin J, Roger P, Marabout B, Sevrin M, Vigé X, Biton B, Steinberg R, Françon D, Alonso R, Avenet P, Oury-Donat F, Perrault G, Griebel G, George P, Soubrié P, Scatton B (2005) Neurochemical, electrophysiological and pharmacological profiles of the selective inhibitor of the glycine transporter-1 SSR504734, a potential new type of antipsychotic. Neuropsychopharmacology 30:1963–1985PubMedCrossRefGoogle Scholar
  29. Ellenbroek BA (2004) Pre-attentive processing and schizophrenia: animal studies. Psychopharmacology (Berl) 174:65–74CrossRefGoogle Scholar
  30. Fox GB, Esbenshade TA, Pan JB, Radek RJ, Krueger KM, Yao BB, Browman KE, Buckley MJ, Ballard ME, Komater VA, Miner H, Zhang M, Faghih R, Rueter LE, Bitner RS, Drescher KU, Wetter J, Marsh K, Lemaire M, Porsolt RD, Bennani YL, Sullivan JP, Cowart MD, Decker MW, Hancock AA (2005) Pharmacological properties of ABT-239 [4-(2-{2-[(2R)-2-methylpyrrolidinyl]ethyl}-benzofuran-5-yl) benzonitrile]: II. Neurophysiological characterization and broad preclinical efficacy in cognition and schizophrenia of a potent and selective histamine H3 receptor antagonist. J Pharmacol Exp Ther 313:176–190PubMedCrossRefGoogle Scholar
  31. Gaisler-Salomon I, Weiner I (2003) Systemic administration of MK-801 produces an abnormally persistent latent inhibition which is reversed by clozapine but not haloperidol. Psychopharmacology (Berl) 166:333–342Google Scholar
  32. Gaisler-Salomon I, Diamant L, Rubin C, Weiner I (2008) Abnormally persistent latent inhibition induced by MK801 is reversed by risperidone and by positive modulators of NMDA receptor function: differential efficacy depending on the stage of the task at which they are administered. Psychopharmacology (Berl) 196:255–267CrossRefGoogle Scholar
  33. Gerlai R (1998) Contextual learning and cue association in fear conditioning in mice: a strain comparison and lesion study. Behav Brain Res 133:925–940Google Scholar
  34. Geyer MA (2006a) The family of sensorimotor gating disorders: comorbidities or diagnostic overlaps? Neurotox Res 10:211–220PubMedCrossRefGoogle Scholar
  35. Geyer MA (2006b) Are cross-species measures of sensorimotor gating useful for the discovery of procognitive cotreatments for schizophrenia? Dialogues Clin Neurosci 8:9–16PubMedGoogle Scholar
  36. Geyer MA, Braff DL (1987) Startle habituation and sensorimotor gating in schizophrenia and related animal models. Schizophr Bull 13:643–668PubMedGoogle Scholar
  37. Geyer MA, McIlwain KL, Paylor R (2002) Mouse genetic models for prepulse inhibition: an early review. Mol Psychiatry 7:1039–1053PubMedCrossRefGoogle Scholar
  38. Geyer MA, Swerdlow NR, Mansbach RS, Braff DL (1990) Startle response models of sensorimotor gating and habituation deficits in schizophrenia. Brain Res Bull 25:485–498PubMedCrossRefGoogle Scholar
  39. Gould TJ, Wehner JM (1999) Genetic influences on latent inhibition. Behav Neurosci 113:1291–1296PubMedCrossRefGoogle Scholar
  40. Gray JA, Feldon J, Rawlins JNP, Hemsley DR, Smith AD (1991) The neuropsychology of schizophrenia. Behav Brain Res 14:1–84Google Scholar
  41. Gray NS, Hemsley DR, Gray JA (1992) Abolition of latent inhibition in acute, but not chronic schizophrenics. Neurol Psychiatry Brain Res 1:83–89Google Scholar
  42. Gray JA, Joseph MH, Hemsley DR, Young AM, Warburton EC, Boulenguez P, Grigoryan GA, Peters SL, Rawlins JN, Taib CT (1995) The role of mesolimbic dopaminergic and retrohippocampal afferents to the nucleus accumbens in latent inhibition: implications for schizophrenia Behav Brain Res 71:19–31Google Scholar
  43. Hince DA, Martin-Iverson MT (2005) Differences in prepulse inhibition (PPI) between Wistar and Sprague–Dawley rats clarified by a new method of PPI standardization. Behav Neurosci 119:66–77PubMedCrossRefGoogle Scholar
  44. Hoffman HS, Searle JL (1965) Acoustic variables in the modification of startle reaction in the rat. J Comp Physiol Psychol 60:53–58PubMedCrossRefGoogle Scholar
  45. Honey RC, Good M (1993) Selective hippocampal lesions abolish the contextual specificity of latent inhibition and conditioning. Behav Neurosci 107:23–33PubMedCrossRefGoogle Scholar
  46. Iso H, Shimai S (1991) Running-wheel avoidance learning in mice (Mus musculus): evidence of contingency learning and differences among inbred strains. J Comp Psychol 105:190–202CrossRefGoogle Scholar
  47. Javitt DC (2007) Glutamate and schizophrenia: phencyclidine, N-methyl-d-aspartate receptors, and dopamine–glutamate interactions. Int Rev Neurobiol 78:69–108PubMedCrossRefGoogle Scholar
  48. Killcross AS, Kiernan MJ, Dwyer D, Westbrook RF (1998) Loss of latent inhibition of contextual conditioning following non-reinforced context exposure in rats. Q J Exp Psychol B 51:75–90PubMedGoogle Scholar
  49. Kinney GG, Sur C, Burno M, Mallorga PJ, Williams JB, Figueroa DJ, Wittmann M, Lemaire W, Conn PJ (2003) The glycine transporter type 1 inhibitor N-[3-(4'-fluorophenyl)-3-(4'-phenylphenoxy) propyl]sarcosine potentiates NMDA receptor-mediated responses in vivo and produces an antipsychotic profile in rodent behavior. J Neurosci 23:7586–7591PubMedGoogle Scholar
  50. Lipina T, Labrie V, Weiner I, Roder J (2005) Modulators of the glycine site on NMDA receptors, d-serine and ALX 5407, display similar beneficial effects to clozapine in mouse models of schizophrenia. Psychopharmacology (Berl) 179:54–67CrossRefGoogle Scholar
  51. 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 80:1075–1086PubMedCrossRefGoogle Scholar
  52. Lubow RE (1989) Latent inhibition and conditioned attention theory. Cambridge University Press, New YorkGoogle Scholar
  53. Lubow RE, Moore AU (1959) Latent inhibition: the effect of non-reinforced preexposure to the conditional stimulus. J Comp Physiol Psychol 66:688–694CrossRefGoogle Scholar
  54. Mackintosh NJ (1973) Stimulus selection: learning to ignore stimuli that predict no change in reinforcement. In: Hinde RA, Stevenson-Hinde J (eds) Constraints on learning. Academic, London, pp 75–96Google Scholar
  55. McCaughran JJ, Mahjubi E, Decena E, Hitzemann R (1997) Genetics, haloperidol-induced catalepsy and haloperidol-induced changes in acoustic startle and prepulse inhibition. Psychopharmacology 134:131–139PubMedCrossRefGoogle Scholar
  56. McNamara RK, Levant B, Taylor B, Ahlbrand R, Liu Y, Sullivan JR, Stanford K, Richtand NM (2006) C57BL/6J mice exhibit reduced dopamine D3 receptor-mediated locomotor-inhibitory function relative to DBA/2J mice. Neuroscience 143:141–153PubMedCrossRefGoogle Scholar
  57. Morse AC, Erwin VG, Jones BC (1993) Strain and housing affect cocaine self-selection and open-field locomotor activity in mice. Pharmacol Biochem Behav 45:905–912PubMedCrossRefGoogle Scholar
  58. Olivier B, Leahy C, Mullen T, Paylor R, Groppi VE, Sarnyai Z, Brunner D (2001) The DBA/2J strain and prepulse inhibition of startle: a model system to test antipsychotics. Psychopharmacology (Berl) 156:284–290CrossRefGoogle Scholar
  59. Paylor R, Baskall L, Wehner JM (1993) Behavioral dissociations between C57BL/6 and DBA/2 mice on learning and memory tasks: a hippocampal dysfunction hypothesis. Psychobiology 21:11–26Google Scholar
  60. Paylor R, Crawley JN (1997) Inbred strain differences in prepulse inhibition of the mouse startle response. Psychopharmacology 132:169–118PubMedCrossRefGoogle Scholar
  61. Paylor R, Tracy R, Wehner J, Rudy JR (1994) DBA/2 and C57BL/6 mice differ in contextual fear conditioning but not auditory fear conditioning. Behav Neurosci 108:810–817PubMedCrossRefGoogle Scholar
  62. Pietropaolo S, Singer P, Feldon J, Yee BK (2008) The postweaning social isolation in C57BL/6 mice: preferential vulnerability in the male sex. Psychopharmacology 197:613–628PubMedCrossRefGoogle Scholar
  63. Pouzet B, Zhang WN, Weiner I, Feldon J, Yee BK (2004) Latent inhibition is spared by N-methyl-d-aspartate (NMDA)-induced ventral hippocampal lesions, but is attenuated following local activation of the ventral hippocampus by intracerebral NMDA infusion. Neuroscience 124:183–194PubMedCrossRefGoogle Scholar
  64. Puglisi-Allegra S, Cabib S (1997) Psychopharmacology of dopamine: the contribution of comparative studies in inbred strains of mice. Prog Neurobiol 51:637–661PubMedCrossRefGoogle Scholar
  65. Oliverio A (1967) Effects of different conditioning schedules based on visual and acoustic conditioned stimulus on avoidance learning of two strains of mice. J Psychol 65:131–139PubMedGoogle Scholar
  66. Ouagazzal AM, Jenck F, Moreau JL (2001) Drug-induced potentiation of prepulse inhibition of acoustic startle reflex in mice: a model for detecting antipsychotic activity? Psychopharmacology (Berl) 156:273–283CrossRefGoogle Scholar
  67. Restivo L, Passino E, Middei S, Ammassari-Teule M (2002) The strain-specific involvement of nucleus accumbens in latent inhibition might depend on differences in processing configural- and cue-based information between C57BL/6 and DBA mice. Brain Res Bull 57:35–39PubMedCrossRefGoogle Scholar
  68. Sandner G, Canal NM (2007) Relationship between PPI and baseline startle response. Cogn Neurodyn 1:27–37PubMedCrossRefGoogle Scholar
  69. Schmajuk NA, Larrauri JA (2005) Neural network model of prepulse inhibition. Behav Neurosci 119:1546–1562PubMedCrossRefGoogle Scholar
  70. Schmajuk NA, Gray JA, Lam YW (1996) Latent inhibition: a neural network approach. J Exp Psychol Anim Behav Process 22:321–349PubMedCrossRefGoogle Scholar
  71. Schiller D, Zuckerman L, Weiner I (2006) Abnormally persistent latent inhibition induced by lesions to the nucleus accumbens core, basolateral amygdala and orbitofrontal cortex is reversed by clozapine but not by haloperidol. J Psychiatr Res 40:167–177PubMedCrossRefGoogle Scholar
  72. Schwabe K, Freudenberg F, Koch M (2007) Selective breeding of reduced sensorimotor gating in Wistar rats. Behav Genet 37:706–712PubMedCrossRefGoogle Scholar
  73. Snyder SH (1976) The dopamine hypothesis of schizophrenia: focus on the dopamine receptor. Am J Psychiatry 133:197–202PubMedGoogle Scholar
  74. Spielewoy C, Markou A (2004) Strain-specificity in nicotine attenuation of phencyclidine-induced disruption of prepulse inhibition in mice: relevance to smoking in schizophrenia patients. Behav Genet 34:343–354PubMedCrossRefGoogle Scholar
  75. Sprott RL, Stavnes K (1975) Effects of situational variables on performance of inbred mice in active- and passive-avoidance situations. Psychol Rep 37:683–692PubMedGoogle Scholar
  76. Stavnes K, Sprott RL (1975a) Effects of age and genotype on acquisition of an active avoidance response in mice. Dev Psychobiol 8:437–445PubMedCrossRefGoogle Scholar
  77. Stavnes KL, Sprott RL (1975b) Genetic analysis of active avoidance performance in mice. Psychol Rep 36:515–521PubMedGoogle Scholar
  78. Stevens KE, Freedman R, Collins AC, Hall M, Leonard S, Marks MJ, Rose GM (1996) Genetic correlation of inhibitory gating of hippocampal auditory evoked response and alpha-bungarotoxin-binding nicotinic cholinergic receptors in inbred mouse strains. Neuropsychopharmacology 15:152–162PubMedCrossRefGoogle Scholar
  79. Stevens KE, Wear KD (1997) Normalizing effects of nicotine and a novel nicotinic agonist on hippocampal auditory gating in two animal models. Pharmacol Biochem Behav 57:869–874PubMedCrossRefGoogle Scholar
  80. Swerdlow NR, Braff DL, Geyer MA (2000) Animal models of deficient sensorimotor gating: what we know, what we think we know, and what we hope to know soon. Behav Pharmacol 11:185–204PubMedGoogle Scholar
  81. Swerdlow NR, Geyer MA (1998) Using an animal model of deficient sensorimotor gating to study the pathophysiology and new treatments of schizophrenia. Schizophr Bull 24:285–301PubMedGoogle Scholar
  82. Swerdlow NR, Weber M, Qu Y, Light GA, Braff DL (2008) Realistic expectations of prepulse inhibition in translational models for schizophrenia research. Psychopharmacology (Berl) 199:331–388CrossRefGoogle Scholar
  83. Tohmi M, Tsuda N, Mizuno M, Takei N, Frankland PW, Nawa H (2005) Distinct influences of neonatal epidermal growth factor challenge on adult neurobehavioral traits in four mouse strains. Behav Genet 35:615–629PubMedCrossRefGoogle Scholar
  84. Ventura R, Alcaro A, Cabib S, Conversi D, Mandolesi L, Puglisi-Allegra S (2004) Dopamine in the medial prefrontal cortex controls genotype-dependent effects of amphetamine on mesoaccumbens dopamine release and locomotion. Neuropsychopharmacology 29:72–80PubMedCrossRefGoogle Scholar
  85. Vetulani J, Battaglia M, Sansone M (1989) Nimodipine on shuttle-box avoidance learning in mice: no impairment but slight improvement. Pharmacol Biochem Behav 56:577–581CrossRefGoogle Scholar
  86. Wagner AR (1978) Expectancies and the priming of STM. In: Tighe TJ, Fowler H, Honig WK (eds) Cognitive processes in animal behavior. Erlbaum, Hillsdale, NJ, pp 177–209Google Scholar
  87. Wahlsten D (1972) Phenotypic and genetic relations between initial response to electric shock and rate of avoidance learning in mice. Behav Genet 2:211–240PubMedCrossRefGoogle Scholar
  88. Wehner JM, Sleight S, Upchurch M (1990) Hippocampal protein kinase C is reduced in poor spatial learners. Brain Res 523:181–187PubMedCrossRefGoogle Scholar
  89. Weinberger SB, Koob GF, Martinez JL Jr (1992) Differences in one-way active avoidance learning in mice of three inbred strains. Behav Genet 22:177–188PubMedCrossRefGoogle Scholar
  90. Weiner I (2003) The "two-headed" latent inhibition model of schizophrenia: modelling positive and negative symptoms and their treatment. Psychopharmacology (Berl) 169:257–297CrossRefGoogle Scholar
  91. Williams JH, Wellman NA, Geaney DP, Cowen PJ, Feldon J, Rawlins JNP (1998) Reduced latent inhibition in people with schizophrenia: an effect of psychosis or of its treatment. Br J Psychiatry 172:243–249PubMedCrossRefGoogle Scholar
  92. Wimer RE, Symington L, Farmer H, Schwartzkroin P (1968) Differences in memory processes between inbred mouse strains C57BL/6J and DBA/2J. J Comp Physiol Psychol 65:126–131PubMedCrossRefGoogle Scholar
  93. Wimer RE, Wimer CC, Vaugh JE, Barber RP, Balvanz BA, Chernow CR (1976) The genetic organization of neuron number in Ammon’s horns of house mouse. Brain Res 118:219–243PubMedCrossRefGoogle Scholar
  94. Yee BK, Feldon J (2009) Distinct forms of prepulse inhibition disruption distinguishable by the associated changes in prepulse-elicited reaction. Behav Brain Res (in press)Google Scholar
  95. Yee BK, Balic E, Singer P, Schwerdel C, Grampp T, Gabernet L, Knuesel I, Benke D, Feldon J, Mohler H, Boison D (2006) Disruption of glycine transporter 1 restricted to forebrain neurons is associated with a procognitive and antipsychotic phenotypic profile. J Neurosci 26:3169–3181PubMedCrossRefGoogle Scholar
  96. Yee BK, Chang DL, Feldon J (2004a) The effects of dizocilpine and phencyclidine on prepulse inhibition of the acoustic startle reflex and on prepulse-elicited reactivity in C57BL6 mice. Neuropsychopharmacology 29:1865–1877PubMedCrossRefGoogle Scholar
  97. Yee BK, Chang T, Pietropaolo P, Feldon J (2005) The expression of prepulse inhibition of the acoustic startle reflex as a function of three pulse stimulus intensities, three prepulse stimulus intensities, and three levels of startle responsiveness in C57BL6/J mice. Behav Brain Res 163:265–276PubMedCrossRefGoogle Scholar
  98. Yee BK, Feldon J, Rawlins JN (1995) Latent inhibition in rats is abolished by NMDA-induced neuronal loss in the retrohippocampal region, but this lesion effect can be prevented by systemic haloperidol treatment. Behav Neurosci 109:227–240PubMedCrossRefGoogle Scholar
  99. Yee BK, Feldon J, Rawlins JN (1997) Cytotoxic lesions of the retrohippocampal region attenuate latent inhibition but spare the partial reinforcement extinction effect. Exp Brain Res 115:247–256PubMedCrossRefGoogle Scholar
  100. Yee BK, Russig H, Feldon J (2004b) Apomorphine-induced prepulse inhibition disruption is associated with a paradoxical enhancement of prepulse stimulus reactivity. Neuropsychopharmacology 29:240–248PubMedCrossRefGoogle Scholar
  101. Zocchi A, Orsini C, Cabib S, Puglisi-Allegra S (1998) Parallel strain-dependent effect of amphetamine on locomotor activity and dopamine release in the nucleus accumbens: an in vivo study in mice. Neuroscience 82:521–528PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Philipp Singer
    • 1
  • Joram Feldon
    • 1
  • Benjamin K. Yee
    • 1
    Email author
  1. 1.Laboratory of Behavioural NeurobiologyFederal Institute of Technology ZurichSchwerzenbachSwitzerland

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