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

Volumn 124, Issue 1, 2004, Pages 183-194

  Pouzet, B ^a,c   Zhang, W N ^a   Weiner, I ^b   Feldon, J ^a   Yee, B K ^a  

^a ETH ZURICH   (Switzerland)

^b TEL AVIV UNIVERSITY   (Israel)

^c H LUNDBECK A S   (Denmark)

Author keywords

Conditioning; Intracerebral infusion; Limbic; Rat; Schizophrenia

Indexed keywords

N METHYL DEXTRO ASPARTIC ACID;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN INJURY; CONDITIONED REFLEX; CONTROLLED STUDY; ENTORHINAL CORTEX; HIPPOCAMPUS; LATENT INHIBITION; MALE; NONHUMAN; PERIKARYON; PREPULSE INHIBITION; PRIORITY JOURNAL; RAT; REGULATORY MECHANISM;

EID: 0442307910     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2003.11.007     Document Type: Article

References (90)

1. Ackil J., Mellgren R.L., Halgren C., Frommer S.P. Effects of CS pre-exposure on avoidance learning in rats with hippocampal lesions. J Comp Physiol Psychol. 69:1969;739-747.
2. Bakshi VP, Geyer MA, Taaid N, Swerdlow (1995) A comparison of the effects of amphetamine, strychnine and caffeine on prepulse inhibition and latent inhibition. Behav Pharmacol 6:801-809.
3. Bartesaghi R. Hippocampal-entorhinal relationships electrophysiological analysis of the ventral hippocampal projections to the ventral entorhinal cortex . Neuroscience. 61:1994;457-466.
4. Bartesaghi R., Gessi T., Sperti L. Electrophysiological analysis of the hippocampal projections to the entorhinal area. Neuroscience. 30:1989;51-62.
5. Baruch I., Hemsley D.R., Gray J.A. Differential performance of acute and chronic schizophrenics in a latent inhibition task. J Nerv Ment Dis. 176:1988;598-606.
6. Bast T., Zhang W.N., Heidbreder C.h, Feldon J. Hyperactivity and disruption of prepulse inhibition induced by N-methyl-D-aspartate stimulation of the ventral hippocampus and the effects of pretreatment with haloperidol and clozapine. Neuroscience. 103:2001;325-335.
7. Bast T., Zhang W.N., Feldon J. Hyperactivity, decreased startle reactivity, and disrupted prepulse inhibition following disinhibition of the rat ventral hippocampus by the GABA(A) receptor antagonist picrotoxin. Psychopharmacology (Berl). 156:2001;225-233.
8. Bazin N., Perruchet P., Hardy-Bayle M.C., Feline A. Context-dependent information processing in patients with schizophrenia. Schizophr Res. 45:2000;93-101.
9. Benes F.M. Emerging principles of altered neural circuitry in schizophrenia. Brain Res Rev. 31:2000;251-269.
10. Bouton M.E. Context, time, and memory retrieval in the interference paradigms of Pavlovian learning. Psychol Bull. 114:1993;80-99.
11. Bouton M.E., Nelson J.B., Rosas J.M. Stimulus generalization, context change, and forgetting. Psychol Bull. 125:1999;171-186.
12. Brog J.S., Salyapongse A., Deutch A.Y., Zahm D.S. The patterns of afferent innervation of the core and shell in the accumbens part of the rat ventral striatum immunohistochemical detection of retrogradely transported fluoro-gold . J Comp Neurol. 338:1993;255-278.
13. Burton H.A., Toga A.W. Successive discrimination performance improves with increasing numbers of stimulus preexposures in septal rats. Behav Neural Biol. 34:1982;141-151.
14. Chrobak J.J., Buzsaki G. Operational dynamics in the hippocampal- entorhinal axis. Neurosci Biobehav Rev. 22:1998;303-310.
15. Clark A.J., Feldon J., Rawlins J.N.P. Aspiration lesions of rat ventral hippocampus disinhibit responding in conditioned suppression or extinction, but spare latent inhibition and the partial reinforcement extinction effect. Neuroscience. 48:1992;821-829.
16. Cohen J.D., Servan-Schreiber D. Context, cortex, and dopamine a connectionist approach to behavior and biology in schizophrenia . Psychol Rev. 99:1992;45-77.
17. Cohen J.D., Braver T.S., O'Reilly R.C. A computational approach to prefrontal cortex, cognitive control and schizophrenia recent developments and current challenges . Philos Trans R Soc Lond B Biol Sci. 351:1996;1515-1527.
18. Cohen J.D., Barch D.M., Carter C., Servan-Schreiber D. Context-processing deficits in schizophrenia converging evidence from three theoretically motivated cognitive tasks . J Abnorm Psychol. 108:1999;120-133.
19. Coutureau E., Galani R., Gosselin O., Majchrzak M., Di Scala G. Entorhinal but not hippocampal or subicular lesions disrupt latent inhibition in rats. Neurobiol Learn Mem. 72:1999;143-157.
20. Depoortere R., Perrault G., Sanger D.J. Potentiation of prepulse inhibition of the startle reflex in rats pharmacological evaluation of the procedure as a model for detecting antipsychotic activity . Psychopharmacology (Berl). 132:1997;366-374.
21. Dunn L.A., Atwater G.E., Kilts C.D. Effects of antipsychotic drugs on latent inhibition sensitivity and specificity of an animal behavioral model of clinical drug action . Psychopharmacology (Berl). 112:1993;315-323.
22. Escobar M., Oberling P., Miller R.R. Associative deficit accounts of disrupted latent inhibition and blocking in schizophrenia. Neurosci Biobehav Rev. 26:2002;203-216.
23. Estes W.K., Skinner B.F. Some quantitative properties of anxiety. J Exp Psychol. 29:1941;390-400.
24. Feldon J., Weiner I. The latent inhibition model of schizophrenic attention disorder haloperidol and sulpiride enhance rats' ability to ignore irrelevant stimuli . Biol Psychiatry. 29:1991;635-646.
25. Floresco S.B., Todd C.L., Grace A.A. Glutamatergic afferents from the hippocampus to the nucleus accumbens regulate activity of ventral tegmental area dopamine neurons. J Neurosci. 21:2001;4915-4922.
26. Gluck M.A., Myers C.E. Psychobiological models of hippocampal function in learning and memory. Annu Rev Psychol. 48:1997;481-514.
27. Grace A.A. Gating of information flow within the limbic system and the pathophysiology of schizophrenia. Brain Res Rev. 31:2000;330-341.
28. Grace A.A., Moore H., O'Donnell P. The modulation of corticoaccumbens transmission by limbic afferents and dopamine a model for the pathophysiology of schizophrenia . Adv Pharmacol. 42:1998;721-724.
29. Grahame N.J., Barnet R.C., Gunther L.M., Miller R.R. Latent inhibition as a performance deficit resulting from CS-context associations. Anim Learn Behav. 22:1994;395-409.
30. Gray N.S., Pickering A.D., Hemsley D.R., Dawling S., Gray J.A. Abolition of latent inhibition by a single 5 mg dose of d-amphetamine in man. Psychopharmacology. 107:1992;425-430.
31. Gray J.A., Feldon J., Rawlins J.N.P., Hemsley D.R., Smith A.D. The neuropsychology of schizophrenia. Behav Brain Sci. 14:1991;1-84.
32. Gray J.A., Joseph M.H., Hemsley D.R., Young A.M., Warburton E.C., Boulenguez P., Grigoryan G.A., Peters S.L., Rawlins J.N., Taib C.T., et al. The role of mesolimbic dopaminergic and retrohippocampal afferents to the nucleus accumbens in latent inhibition implications for schizophrenia . Behav Brain Res. 71:1995;19-31.
33. Groenewegen H.J., Vermeulen-Van der Zee E., te Kortschot A., Witter M.P. Organization of the projections from the subiculum to the ventral striatum in the rat a study using anterograde transport of Phaseolus vulgaris leucoagglutinin . Neuroscience. 23:1987;103-120.
34. Hamm A.O., Weike A.I., Schupp H.T. The effect of neuroleptic medication on prepulse inhibition in schizophrenia patients current status and future issues . Psychopharmacology (Berl). 156:2001;259-265.
35. Heckers S. Neuroimaging studies of the hippocampus in schizophrenia. Hippocampus. 11:2001;520-528.
36. Hemsley D.R. A simple (or simplistic?) cognitive model for schizophrenia. Behav Res Ther. 31:1993;633-645.
37. Holt W., Maren S. Muscimol inactivation of the dorsal hippocampus impairs contextual retrieval of fear memory. J Neurosci. 19:1999;9054-9062.
38. Honey R.C., Good M. Selective hippocampal lesions abolish the contextual specificity of latent inhibition and conditioning. Behav Neurosci. 107:1993;23-33.
39. Kaye H., Pearce J.M. Hippocampal lesions attenuate latent inhibition and the decline of the orienting response in rats. Q J Exp Psychol B. 39:1987;107-125.
40. Kelley A.E., Domesick V.B. The distribution of the projection from the hippocampal formation to the nucleus accumbens in the rat an anterograde- and retrograde-horseradish peroxidase study . Neuroscience. 7:1982;2321-2335.
41. Killcross A.S., Kiernan M.J., Dwyer D., Westbrook R.F. Loss of latent inhibition of contextual conditioning following non-reinforced context exposure in rats. Q J Exp Psychol B. 51:1998;75-90.
42. Kilts C.D. The changing roles and targets for animal models of schizophrenia. Biol Psychiatry. 50:2001;845-855.
43. Kohler C.H. Intrinsic projections of the retrohippocampal region in the rat brain I. The subicular complex . J Comp Neurol. 236:1985;504-522.
44. Kraemer P.J., Spear N.E. The effect of nonreinforced stimulus preexposure on the strength of a conditioned taste aversion as a function of retention interval do latent inhibition and extinction involve a shared process? Anim Learn Behav. 20:1992;1-7.
45. Kraemer P.J., Spear N.E. Retrieval process and conditioning. Zentall T.R. Animal cognition: a tribute to Donald A. Riley. 1993;87-110 Erlbaum, Hillsdale, NJ.
46. Levita L., Dalley J.W., Robbins T.W. Disruption of Pavlovian contextual conditioning by excitotoxic lesions of the nucleus accumbens core. Behav Neurosci. 116:2002;539-552.
47. Lubow R.E., Gewirtz J.C. Latent inhibition in humans data, theory, and implications for schizophrenia . Psychol Bull. 117:1995;87-103.
48. Lubow R.E., Moore A.U. Latent inhibition the effect of non-reinforced preexposure to the conditional stimulus . J Comp Physiol Psych. 52:1959;415-419.
49. Lubow R.E. Latent inhibition and conditioned attention theory. 1989;Cambridge University Press, Cambridge.
50. Mackintosh N.J. The psychology of animal learning. 1974;Academic Press, New York.
51. McLaren I.P.L., Mackintosh N.J. An elemental model of associative learning I. Latent inhibition and perceptual learning . Anim Learn Behav. 28:2000;211-246.
52. Miller R.R., Matzel L.D. The comparator hypothesos: a response rule for the expression of associations. Bower G.H. The psychology of learning and motivation, Vol. 22. 1988;51-92 Academic Press, San Diego, CA.
53. Mitchell S.N., Yee B.K., Feldon J., Gray J.A., Rawlins J.N.P. Activation of the retrohippocampal region in the rat causes dopamine release in the nucleus accumbens disruption by fornix section . Eur J Pharmacol. 407:2000;131-138.
54. Murphy C.A., Fend M., Russig H., Feldon J. Latent inhibition, but not prepulse inhibition, is reduced during withdrawal from an escalating dosage schedule of amphetamine. Behav Neurosci. 115:2001;1247-1256.
55. Newman R., Winans S.S. An experimental study of the ventral striatum of the golden hamster I. Neuronal connections of the nucleus accumbens . J Comp Neurol. 191:1980;167-192.
56. O'Donnell P., Grace A.A. Synaptic interactions among excitatory afferents to nucleus accumbens neurons hippocampal gating of prefrontal cortical input . J Neurosci. 15:1995;3622-3639.
57. O'Donnell P., Grace A.A. Dysfunctions in multiple interrelated systems as the neurobiological bases of schizophrenic symptom clusters. Schizophr Bull. 24:1998;267-283.
58. O'Donnell P., Greene J., Pabello N., Lewis B.L., Grace A.A. Modulation of cell firing in the nucleus accumbens. Ann NY Acad Sci. 877:1999;157-175.
59. Paxinos G., Watson C. The rat brain in stereotaxic coordinates, 2nd edition. 1986;Academic Press, New York.
60. Phillipson O.T., Griffiths A.C. The topographic order of inputs to nucleus accumbens in the rat. Neuroscience. 16:1985;275-296.
61. Pouzet B., Veenman C.L., Yee B.K., Feldon J., Weiner I. The effects of radiofrequency lesion or transection of the fimbria-fornix on latent inhibition in the rat. Neuroscience. 91:1999;1355-1368.
62. Purves D., Bonardi C., Hall G. Enhancement of latent inhibition in rats with electrolytic lesions of the hippocampus. Behav Neurosci. 109:1995;366-370.
63. Reilly S., Harley C., Revusky S. Ibotenate lesions of the hippocampus enhance latent inhibition in conditioned taste aversion and increase resistance to extinction in conditioned taste preference. Behav Neurosci. 107:1993;996-1004.
64. Richmond M.A., Yee B.K., Pouzet B., Veenman L., Rawlins J.N., Feldon J., Bannerman D.M. Dissociating context and space within the hippocampus effects of complete, dorsal, and ventral excitotoxic hippocampal lesions on conditioned freezing and spatial learning . Behav Neurosci. 113:1999;1189-1203.
65. Servan-Schreiber D., Cohen J.D., Steingard S. Schizophrenic deficits in the processing of context a test of a theoretical model . Arch Gen Psychiatry. 53:1996;1105-1112.
66. Sesack S.R., Pickel V.M. In the rat medial nucleus accumbens, hippocampal and catecholaminergic terminals converge on spiny neurons and are in apposition to each other. Brain Res. 527:1990;266-279.
67. Shenton M.E., Dickey C.C., Frumin M., McCarley R.W. A review of MRI findings in schizophrenia. Schizophr Res. 49:2001;1-52.
68. Swerdlow N.R., Geyer M.A. Using an animal model of deficient sensorimotor gating to study the pathophysiology and new treatments of schizophrenia. Schizophr Bull. 24:1998;285-301.
69. Swerdlow N.R., Braff D.L., Taaid N., Geyer M.A. Assessing the validity of an animal model of deficient sensorimotor gating in schizophrenic patients. Arch Gen Psychiatry. 51:1994;139-154.
70. Swerdlow N.R., Taaid N., Halim N., Randolph E., Kim Y.K., Auerbach P. Hippocampal lesions enhance startle gating-disruptive effects of apomorphine in rats a parametric assessment . Neuroscience. 96:2000;523-536.
71. Tai C.T., Cassaday H.J., Feldon J., Rawlins J.N.P. Both electrolytic and excitotoxic lesions of nucleus accumbens disrupt latent inhibition of learning in rats. Neurobiol Learn Mem. 64:1995;36-48.
72. Toga A.W., Burton H.A. Effects of the lateral septum and latent inhibition on successive discrimination learning. J Neurosci Res. 4:1979;215-224.
73. Totterdell S., Smith A.D. Convergence of hippocampal and dopaminergic input onto identified neurons in the nucleus accumbens of the rat. J Chem Neuroanat. 2:1989;285-298.
74. Totterdell S., Meredith G.E. Topographical organization of projections from the entorhinal cortex to the striatum of the rat. Neuroscience. 78:1997;715-729.
75. Varty G.B., Walters N., Cohen-Williams M., Carey G.J. Comparison of apomorphine, amphetamine and dizocilpine disruptions of prepulse inhibition in inbred and outbred mice strains. Eur J Pharmacol. 424:2001;27-36.
76. Wagner AR (1978) Expectancies and the priming of STM. In: Cognitive processes in animal behavior (Tighe TJ, Fowler H, Honig WK, eds), pp 177-210. Hilldsdale, NJ: Erlbaum.
77. Warburton E.C., Joseph M.H., Feldon J., Weiner I., Gray J.A. Antagonism of amphetamine-induced disruption of latent inhibition in rats by haloperidol and ondansetron implications for a possible antipsychotic action of ondansetron . Psychopharmacology (Berl). 114:1994;657-664.
78. Weiner I. Neural substrates of latent inhibition the switching model . Psychol Bull. 108:1990;442-461.
79. Weiner I. The "two-headed" latent inhibition model of schizophrenia modeling positive and negative symptoms and their treatment . Psychopharmacology. 169:2003;257-297.
80. Weiner I., Gal G., Rawlins J.N., Feldon J. Differential involvement of the shell and core subterritories of the nucleus accumbens in latent inhibition and amphetamine-induced activity. Behav Brain Res. 81:1996;123-133.
81. Weiner I., Gal G., Feldon J. Disrupted and undisruptable latent inhibition following shell and core lesions. Ann NY Acad Sci. 877:1999;723-727.
82. Weiss K.R., Friedman R., McGregor S. Effects of septal lesions on latent inhibition and habituation of the orienting response in rats. Acta Neurobiol Exp. 34:1974;491-504.
83. Weiss I.C., Domeney A.M., Moreau J.L., Russig H., 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. Behav Brain Res. 121:2001;207-218.
84. Witter M.P., Groenewegen H.J., Lopes da Silva F.H., Lohman A.H. Functional organization of the extrinsic and intrinsic circuitry of the parahippocampal region. Prog Neurobiol. 33:1989;161-253.
85. Yee B.K., Feldon J., Rawlins J.N.P. 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. 109:1995;227-240.
86. Yee B.K., Feldon J., Rawlins J.N.P. Potentiation of amphetamine-induced locomotor activity following NMDA-induced retrohippocampal neuronal loss in the rat. Exp Brain Res. 106:1995;356-364.
87. Yee B.K., Feldon J., Rawlins J.N.P. Cytotoxic lesions of the retrohippocampal region attenuate latent inhibition but spare the partial reinforcement extinction effect. Exp Brain Res. 115:1997;247-256.
88. Zhang W., Pouzet B., Jongen-Rêlo A.L., Weiner I., Feldon J. 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. 10:1999;2533-2538.
89. Zhang W.N., Bast T., Feldon J. The ventral hippocampus and fear conditioning in rats different anterograde amnesias of fear after infusion of N-methyl-D-aspartate or its noncompetitive antagonist MK-801 into the ventral hippocampus . Behav Brain Res. 126:2001;159-174.
90. Zhang W.N., Bast T., Feldon J. Effects of hippocampal N-methyl-D-aspartate infusion on locomotor activity and prepulse inhibition differences between the dorsal and ventral hippocampus. Behav Neurosci. 116:2002;72-84.