Postnatal functional inactivation of the entorhinal cortex or ventral subiculum has different consequences for latent inhibition-related striatal dopaminergic responses in adult rats

European Journal of Neuroscience

Volumn 29, Issue 10, 2009, Pages 2035-2048

  Meyer, F ^a   Peterschmitt, Y ^a,b   Louilot, A ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b MEDICAL UNIVERSITY OF VIENNA   (Austria)

Author keywords

Anterior dorsal striatum; Conditioned olfactory aversion; In vivo voltammetry; Recognition memory; Schizophrenia

Indexed keywords

DOPAMINE; PHOSPHATE BUFFERED SALINE; TETRODOTOXIN;

ANIMAL TISSUE; ARTICLE; BRAIN LEVEL; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINE RELEASE; DOPAMINERGIC ACTIVITY; ENTORHINAL CORTEX; FEMALE; IN VIVO STUDY; LATENT INHIBITION; LATENT PERIOD; MALE; NERVE CELL INHIBITION; NEWBORN; NONHUMAN; POSTNATAL DEVELOPMENT; POTENTIOMETRY; PRIORITY JOURNAL; RAT; SCHIZOPHRENIA; SUBICULUM; TISSUE STRUCTURE;

ANIMALS; BEHAVIOR, ANIMAL; CORPUS STRIATUM; DOPAMINE; ENTORHINAL CORTEX; FEMALE; HIPPOCAMPUS; INHIBITION (PSYCHOLOGY); MALE; NEUROGENESIS; POISONS; RATS; RATS, SPRAGUE-DAWLEY; SCHIZOPHRENIA; TETRODOTOXIN;

EID: 65749120700     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2009.06755.x     Document Type: Article

References (98)

1. Abi-Dargham, A., Gil, R., Krystal, J., Baldwin, R.M., Seibyl, J.P., Bowers, M., van Dyck, C.H., Charney, D.S., Innis, R.B. Laruelle, M. (1998) Increased striatal dopamine transmission in schizophrenia: confirmation in a second cohort. Am. J. Psychiatry, 155, 761 767. (Pubitemid 28252654)
2. Ambrogi Lorenzini, C.G., Baldi, E., Bucherelli, C., Sacchetti, B. Tassoni, G. (1997) Role of ventral hippocampus in acquisition, consolidation and retrieval of rat's passive avoidance response memory trace. Brain Res., 768, 242 248. (Pubitemid 27433497)
3. Angst, M.J., Macedo, C.E., Guiberteau, T. Sandner, G. (2007) Alteration of conditioned emotional response and conditioned taste aversion after neonatal ventral hippocampus lesions in rats. Brain Res., 1143, 183 192. (Pubitemid 46440810)
4. Antonini, A. Stryker, M.P. (1993) Development of individual geniculocortical arbors in cat striate cortex and effects of binocular impulse blockade. J. Neurosci., 13, 3549 3573. (Pubitemid 23241190)
5. Arnold, S.E. (2000) Cellular and molecular neuropathology of the parahippocampal region in schizophrenia. Ann. NY Acad. Sci., 911, 275 292. (Pubitemid 30462088)
6. Arnold, S.E., Hyman, B.T., Van Hoesen, G.W. Damasio, A.R. (1991) Some cytoarchitectural abnormalities of the entorhinal cortex in schizophrenia. Arch. Gen. Psychiatry, 48, 625 632.
7. Arnold, S.E., Franz, B.R., Gur, R.C., Gur, R.E., Shapiro, R.M., Moberg, P.J. Trojanowski, J.Q. (1995) Smaller neuron size in schizophrenia in hippocampal subfields that mediate cortical-hippocampal interactions. Am. J. Psychiatry, 152, 738 748.
8. Arnold, S.E., Talbot, K. Hahn, C.G. (2005) Neurodevelopment, neuroplasticity, and new genes for schizophrenia. Prog. Brain Res., 147, 319 345.
9. Barres, B.A. Raff, M.C. (1993) Proliferation of oligodendrocyte precursor cells depends on electrical activity in axons. Nature, 361, 258 260. (Pubitemid 23034475)
10. Baruch, I., Hemsley, D.R. Gray, J.A. (1988) Differential performance of acute and chronic schizophrenics in a latent inhibition task. J. Nerv. Ment. Dis., 176, 598 606. (Pubitemid 18250872)
11. Beckmann, H. Jakob, H. (1991) Prenatal disturbances of nerve cell migration in the entorhinal region: a common vulnerability factor in functional psychoses? J. Neural Transm. Gen. Sect., 84, 155 164.
12. Besson, C. Louilot, A. (1995) Asymmetrical involvement of mesolimbic dopaminergic neurons in affective perception. Neuroscience, 68, 963 968.
13. Besson, C. Louilot, A. (1997) Striatal dopaminergic changes depend on the attractive or aversive value of stimulus. Neuroreport, 8, 3523 3526. (Pubitemid 27497476)
14. Bouton, M.E. (1993) Context, time, and memory retrieval in the interference paradigms of Pavlovian learning. Psychol. Bull., 114, 80 99.
15. Breier, A., Su, T.P., Saunders, R., Carson, R.E., Kolachana, B.S., de Bartolomeis, A., Weinberger, D.R., Weisenfeld, N., Malhotra, A.K., Eckelman, W.C. Pickar, D. (1997) Schizophrenia is associated with elevated amphetamine-induced synaptic dopamine concentrations: evidence from a novel positron emission tomography method. Proc. Natl Acad. Sci. USA, 94, 2569 2574. (Pubitemid 27136916)
16. Bullmore, E.T., Frangou, S. Murray, R.M. (1997) The dysplastic net hypothesis: an integration of developmental and dysconnectivity theories of schizophrenia. Schizophr. Res., 28, 143 156. (Pubitemid 28055662)
17. Carlsson, A., Waters, N., Holm-Waters, S., Tedroff, J., Nilsson, M. Carlsson, M.L. (2001) Interactions between monoamines, glutamate, and GABA in schizophrenia: new evidence. Annu. Rev. Pharmacol. Toxicol., 41, 237 260. (Pubitemid 32385889)
18. Clancy, B., Darlington, R.B. Finlay, B.L. (2001) Translating developmental time across mammalian species. Neuroscience, 105, 7 17. (Pubitemid 32722089)
19. Dao-Castellana, M.H., Paillère-Martinot, M.L., Hantraye, P., Attar-Lévy, D., Rémy, P., Crouzel, C., Artiges, E., Féline, A., Syrota, A. Martinot, J.L. (1997) Presynaptic dopaminergic function in the striatum of schizophrenic patients. Schizophr. Res., 23, 167 174. (Pubitemid 27106901)
20. Demerens, C., Stankoff, B., Logak, M., Anglade, P., Allinquant, B., Couraud, F., Zalc, B. Lubetzki, C. (1996) Induction of myelination in the central nervous system by electrical activity. Proc. Natl Acad. Sci. USA, 93, 9887 9892. (Pubitemid 26296704)
21. Drakew, A., Frotscher, M. Heimrich, B. (1999) Blockade of neuronal activity alters spine maturation of dentate granule cells but not their dendritic arborization. Neuroscience, 94, 767 774. (Pubitemid 29474964)
22. Falkai, P., Schneider-Axmann, T. Honer, W.G. (2000) Entorhinal cortex pre-alpha cell clusters in schizophrenia: quantitative evidence of a developmental abnormality. Biol. Psychiatry, 47, 937 943. (Pubitemid 30320738)
23. Finch, D.M. (1996) Neurophysiology of converging synaptic inputs from the rat prefrontal cortex, amygdala, midline thalamus, and hippocampal formation onto single neurons of the caudate/putamen and nucleus accumbens. Hippocampus, 6, 495 512. (Pubitemid 26413936)
24. Finch, D.M., Gigg, J., Tan, A.M. Kosoyan, O.P. (1995) Neurophysiology and neuropharmacology of projections from entorhinal cortex to striatum in the rat. Brain Res., 670, 233 247.
25. Flecknell, P.A. (1987) Laboratory Animal Anaesthesia: An Introduction for Research Workers and Technicians. Academic Press, San Diego, CA.
26. Foucher, J.R., Vidailhet, P., Chanraud, S., Gounot, D., Grucker, D., Pins, D., Damsa, C. Danion, J.M. (2005) Functional integration in schizophrenia: too little or too much? Preliminary results on fMRI data Neuroimage, 26, 374 388. (Pubitemid 40719818)
27. Fricke, R. Cowan, W.M. (1978) An autoradiographic study of the development of the entorhinal and commissural afferents of the dentate gyrus of the rat. J. Comp. Neurol., 173, 231 250. (Pubitemid 8396454)
28. Friston, K.J. (1998) The disconnection hypothesis. Schizophr. Res., 30, 115 125. (Pubitemid 28156976)
29. Frotscher, M., Drakew, A. Heimrich, B. (2000) Role of afferent innervation and neuronal activity in dendritic development and spine maturation of fascia dentata granule cells. Cereb. Cortex, 10, 946 951.
30. Garcia, J., Lasiter, P.S., Bermudez-Rattoni, F. Deems, D.A. (1985) A general theory of aversion learning. Ann. NY Acad. Sci., 443, 8 21. (Pubitemid 15074665)
31. Gonon, F.G., Navarre, F. Buda, M.J. (1984) In vivo monitoring of dopamine release in the rat brain with differential normal pulse voltammetry. Anal. Chem., 56, 573 575. (Pubitemid 14106520)
32. Gonzalez-Mora, J.L., Guadalupe, T., Fumero, B. Mas, M. (1991) Mathematical resolution of mixed in vivo voltammetry signals. Models, equipment, assessment by simultaneous microdialysis sampling. J. Neurosci. Methods, 39, 231 244.
33. Gray, N.S., Hemsley, D.R. Gray, J.A. (1992) Abolition of latent inhibition in acute, but not chronic, schizophrenics. Neurol. Psychiatry Brain Res., 1, 83 89. (Pubitemid 24025553)
34. Gray, N.S., Pilowsky, L.S., Gray, J.A. Kerwin, R.W. (1995) Latent inhibition in drug naive schizophrenics: relationship to duration of illness and dopamine D2 binding using SPECT. Schizophr. Res., 17, 95 107.
35. Grecksch, G., Bernstein, H.G., Becker, A., Höllt, V. Bogerts, B. (1999) Disruption of latent inhibition in rats with postnatal hippocampal lesions. Neuropsychopharmacology, 20, 525 532. (Pubitemid 29189257)
36. Groenewegen, G.H.J., Vermeulen-Van der Zee, E., te Kortschot, A. Witter, M.P. (1987) 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, 103 120. (Pubitemid 17159558)
37. Harrison, P.J. (1999) The neuropathology of schizophrenia. A critical review of the data and their interpretation. Brain, 122, 593 624. (Pubitemid 29158770)
38. Hietala, J., Syvälahti, E., Vuorio, K., Räkköläinen, V., Bergman, J., Haaparanta, M., Solin, O., Kuoppamäki, M., Kirvelä, O., Ruotsalainen, U. Salokangas, R.K.R. (1995) Presynaptic dopamine function in striatum of neuroleptic-naive schizophrenic patients. Lancet, 346, 1130 1131.
39. Hietala, J., Syvälahti, E., Vilkman, H., Vuorio, K., Räkköläinen, V., Bergman, J., Haaparanta, M., Solin, O., Kuoppamäki, M., Eronen, E., Ruotsalainen, U. Salokangas, R.K.R. (1999) Depressive symptoms and presynaptic dopamine function in neuroleptic-naive schizophrenia. Schizophr. Res., 35, 41 50. (Pubitemid 29023553)
40. Hoover, W.B. Vertes, R.P. (2007) Anatomical analysis of afferent projections to the medial prefrontal cortex in the rat. Brain Struct. Funct., 212, 149 179. (Pubitemid 47394494)
41. Horvitz, J.C. (2000) Mesolimbocortical and nigrostriatal dopamine responses to salient non-reward events. Neuroscience, 96, 651 656. (Pubitemid 30155729)
42. Hutchins, B.I. Kalil, K. (2008) Differential outgrowth of axons and their branches is regulated by localized calcium transients. J. Neurosci., 28, 143 153.
43. Insausti, R., Herrero, M.T. Witter, M.P. (1997) Entorhinal cortex of the rat: cytoarchitectonic subdivisions and the origin and distribution of cortical efferents. Hippocampus, 7, 146 183. (Pubitemid 27192399)
44. Jakob, H. Beckmann, H. (1994) Circumscribed malformation and nerve cell alterations in the entorhinal cortex of schizophrenics. Pathogenetic and clinical aspects. J. Neural Transm. Gen. Sect., 98, 83 106.
45. Jay, T.M. Witter, M.P. (1991) Distribution of hippocampal CA1 and subicular efferents in the prefrontal cortex of the rat studied by means of anterograde transport of Phaseolus vulgaris-leucoagglutinin. J. Comp. Neurol., 313, 574 586.
46. Jay, T.M., Glowinski, J. Thierry, A.M. (1989) Selectivity of the hippocampal projection to the prelimbic area of the prefrontal cortex in the rat. Brain Res., 505, 337 340. (Pubitemid 20013176)
47. Jay, T.M., Thierry, A.M., Wiklund, L. Glowinski, J. (1992) Excitatory amino acid pathway from the hippocampus to the prefrontal cortex. contribution of AMPA receptors in hippocampo-prefrontal cortex transmission. Eur. J. Neurosci., 4, 1285 1295. (Pubitemid 23044623)
48. Jeanblanc, J., Hoeltzel, A. Louilot, A. (2002) Dissociation in the involvement of dopaminergic neurons innervating the core and shell subregions of the nucleus accumbens in latent inhibition and affective perception. Neuroscience, 111, 315 323. (Pubitemid 34449698)
49. Jeanblanc, J., Hoeltzel, A. Louilot, A. (2003) Differential involvement of dopamine in the anterior and posterior parts of the dorsal striatum in latent inhibition. Neuroscience, 118, 233 241. (Pubitemid 36369546)
50. Jeanblanc, J., Peterschmitt, Y., Hoeltzel, A. Louilot, A. (2004) Influence of the entorhinal cortex on accumbal and striatal dopaminergic responses in a latent inhibition paradigm. Neuroscience, 128, 187 200. (Pubitemid 39140692)
51. Karreman, M. Moghaddam, B. (1996) The prefrontal cortex regulates the basal release of dopamine in the limbic striatum: an effect mediated by ventral tegmental area. J. Neurochem., 66, 589 598. (Pubitemid 26036693)
52. Katz, L.C. Shatz, C.J. (1996) Synaptic activity and the construction of cortical circuits. Science, 274, 1133 1138. (Pubitemid 26389269)
53. Kegeles, L.S., Abi-Dargham, A., Zea-Ponce, Y., Rodenhiser-Hill, J., Mann, J.J., Van Heertum, R.L., Cooper, T.B., Carlsson, A. Laruelle, M. (2000) Modulation of amphetamine-induced striatal dopamine release by ketamine in humans: implications for schizophrenia. Biol. Psychiatry, 48, 627 640.
54. Kerr, K.M., Agster, K.L., Furtak, S.C. Burwell, R.D. (2007) Functional neuroanatomy of the parahippocampal region: the lateral and medial entorhinal areas. Hippocampus, 17, 697 708. (Pubitemid 47493452)
55. Laruelle, M., Abi-Dargham, A., van Dyck, C.H., Gil, R., D'Souza, C.D., Erdos, J., McCance, E., Rosenblatt, W., Fingado, C., Zoghbi, S.S., Baldwin, R.M., Seibyl, J.P., Krystal, J.H., Charney, D.S. Innis, R.B. (1996) Single photon emission computerized tomography imaging of amphetamine-induced dopamine release in drug-free schizophrenic subjects. Proc. Natl Acad. Sci. USA, 93, 9235 9240. (Pubitemid 26282047)
56. Laruelle, M., Frankle, W.G., Narendran, R., Kegeles, L.S. Abi-Dargham, A. (2005) Mechanism of action of antipsychotic drugs: from dopamine D(2) receptor antagonism to glutamate NMDA facilitation. Clin. Ther., 27, 16 24. (Pubitemid 41356605)
57. Lewis, M.C. Gould, T.J. (2007) Reversible inactivation of the entorhinal cortex disrupts the establishment and expression of latent inhibition of cued fear conditioning in C57BL/6 mice. Hippocampus, 17, 462 470. (Pubitemid 46897979)
58. Lewis, D.A. Levitt, P. (2002) Schizophrenia as a disorder of neurodevelopment. Annu. Rev. Neurosci., 25, 409 432. (Pubitemid 34748023)
59. Lindström, L.H., Gefvert, O., Hagberg, G., Lundberg, T., Bergström, M., Hartvig, P. Långström, B. (1999) Increased dopamine synthesis rate in medial prefrontal cortex and striatum in schizophrenia indicated by L-(beta-11C) DOPA and PET. Biol. Psychiatry, 46, 681 688. (Pubitemid 29401864)
60. Lipska, B.K., Halim, N.D., Segal, P.N. Weinberger, D.R. (2002) Effects of reversible inactivation of the neonatal ventral hippocampus on behaviour in the adult rat. J. Neurosci., 22, 2835 2842. (Pubitemid 37465832)
61. Louilot, A. Besson, C. (2000) Specificity of amygdalostriatal interactions in the involvement of mesencephalic dopaminergic neurons in affective perception. Neuroscience, 96, 73 82. (Pubitemid 30103605)
62. Louilot, A. Le Moal, M. (1994) Lateralized interdependence between limbicotemporal and ventrostriatal dopaminergic transmission. Neuroscience, 59, 495 500. (Pubitemid 24131506)
63. Louilot, A., Gonon, F., Buda, M., Simon, H., Le Moal, M. Pujol, J.F. (1985) Effects of d- and l-amphetamine on DA metabolism and ascorbic acid levels in nucleus accumbens and olfactory tubercle as studied by in vivo differential pulse voltammetry. Brain Res., 336, 253 263. (Pubitemid 15008375)
64. Louilot, A., Serrano, A. D'Angio, M. (1987) A novel carbon fiber implantation assembly for cerebral voltammetric measurements in freely moving rats. Physiol. Behav., 41, 227 231. (Pubitemid 18022128)
65. Louilot, A., Gonzalez-Mora, J.L., Guadalupe, T. Mas, M. (1991) Sex-related olfactory stimuli induce a selective increase in DA release in the nucleus accumbens of male rats. A voltammetric study. Brain Res., 553, 313 317.
66. Lubow, R.E. (1989) Latent Inhibition and Conditioned Attention Theory. Cambridge University Press, New York.
67. Lubow, R.E. Moore, A.U. (1959) Latent inhibition: the effect of non-reinforced pre-exposure to the conditioned stimulus. J. Comp. Physiol. Psychol., 52, 415 419.
68. Lubow, R.E., Kaplan, O., Abramovich, P., Rudnick, A. Laor, N. (2000) Visual search in schizophrenia: latent inhibition and novel pop-out effects. Schizophr. Res., 45, 145 156.
69. Martin, J.H. Ghez, C. (1993) Differential impairments in reaching and grasping produced by local inactivation within the forelimb representation of the motor cortex in the cat. Exp. Brain Res., 94, 429 443. (Pubitemid 23218100)
70. McGeorge, A.J. Faull, R.L. (1989) The organization of the projection from the cerebral cortex to the striatum in the rat. Neuroscience, 29, 503 537. (Pubitemid 19167370)
71. Naber, P.A., Witter, M.P. Lopes Silva, F.H. (2000) Networks of the hippocampal memory system of the rat. The pivotal role of the subiculum. Ann. NY Acad. Sci., 911, 392 403. (Pubitemid 30462095)
72. O'Mara, S. (2005) The subiculum: what it does, what it might do, and what neuroanatomy has yet to tell us. J. Anat., 207, 271 282. (Pubitemid 41301002)
73. O'Neill, R.D., Lowry, J.P. Mas, M. (1998) Monitoring brain chemistry in vivo: voltammetric techniques, sensors, and behavioral applications. Crit. Rev. Neurobiol., 12, 69 127. (Pubitemid 28177264)
74. Paxinos, G. Watson, C. (1998) The Rat Brain in Stereotaxic Coordinates, 4th Edn. Academic Press, San Diego.
75. Peterschmitt, Y., Hoeltzel, A. Louilot, A. (2005) Striatal dopaminergic responses observed in latent inhibition are dependent on the hippocampal ventral subicular region. Eur. J. Neurosci., 22, 2059 2068. (Pubitemid 41579394)
76. Peterschmitt, Y., Meyer, F. Louilot, A. (2007) Neonatal functional blockade of the entorhinal cortex results in disruption of accumbal dopaminergic responses observed in latent inhibition paradigm in adult rats. Eur. J. Neurosci., 8, 2504 2513. (Pubitemid 46625932)
77. Peterschmitt, Y., Meyer, F. Louilot, A. (2008) Differential influence of the ventral subiculum on dopaminergic responses observed in core and dorsomedial shell subregions of the nucleus accumbens in latent inhibition. Neuroscience, 154, 898 910.
78. Petrulis, A., Alvarez, P. Eichenbaum, H. (2005) Neural correlates of social odor recognition and the representation of individual distinctive social odors within entorhinal cortex and ventral subiculum. Neuroscience, 130, 259 274. (Pubitemid 39550432)
79. Rascle, C., Mazas, O., Vaiva, G., Tournant, M., Raybois, O., Goudemand, M. Thomas, P. (2001) Clinical features of latent inhibition in schizophrenia. Schizophr. Res., 51, 149 161. (Pubitemid 32772848)
80. Rothfeld, J.M., Harlan, R.E., Shivers, B.D. Pfaff, D.W. (1986) Reversible disruption of lordosis via midbrain infusions of procaine and tetrodotoxin. Pharmacol. Biochem. Behav., 25, 857 863. (Pubitemid 17179905)
81. Saunders, R.C., Kolachana, B.S., Bachevalier, J. Weinberger, D.R. (1998) Neonatal lesions of the medial temporal lobe disrupt prefrontal cortical regulation of striatal dopamine. Nature, 393, 169 171. (Pubitemid 28242256)
82. Schlessinger, A.R., Cowan, W.M. Gottlieb, D.I. (1975) An autoradiographic study of the time of origin and the pattern of granule cell migration in the dentate gyrus of the rat. J. Comp. Neurol., 159, 149 175.
83. Schmadel, S., Schwabe, K. Koch, M. (2004) Effects of neonatal excitotoxic lesions of the entorhinal cortex on cognitive functions in the adult rat. Neuroscience, 128, 365 374. (Pubitemid 39200483)
84. Schultz, W. (2007) Multiple dopamine functions at different time courses. Annu. Rev. Neurosci., 30, 259 288. (Pubitemid 47218758)
85. Singh, S.C. (1977a) Comparison of electron microscopy and silver staining for the detection of the first entorhinal synapses to develop in the dentate gyrus. Anat. Embryol. (Berl), 151, 71 89. (Pubitemid 8160223)
86. Singh, S.C. (1977b) The development of olfactory and hippocampal pathways in the brain of the rat. Anat. Embryol. (Berl), 151, 183 199. (Pubitemid 8185629)
87. Stryker, M.P. Harris, W.A. (1986) Binocular impulse blockade prevents the formation of ocular dominance columns in cat visual cortex. J. Neurosci., 6, 2117 2133. (Pubitemid 16043655)
88. Suzuki, W.A. Eichenbaum, H. (2000) The neurophysiology of memory. Ann. NY Acad. Sci., 911, 175 191. (Pubitemid 30462082)
89. Swerdlow, N.R. Koob, G.F. (1987) DA, schizophrenia, mania, and depression: toward a unified hypothesis of cortico-striato-pallido-thalamic function. Behav. Brain Sci., 10, 197 245.
90. Taber, M.T. Fibiger, H.C. (1993) Electrical stimulation of the medial prefrontal cortex increases dopamine release in the striatum. Neuropsychopharmacology, 4, 271 275. (Pubitemid 23363193)
91. Totterdell, S. Meredith, G.E. (1997) Topographical organization of projections from the entorhinal cortex to the striatum of the rat. Neuroscience, 78, 715 729. (Pubitemid 27179654)
92. Uehara, T., Tanii, Y., Sumiyoshi, T. Kurachi, M. (2000) Neonatal lesions of the left entorhinal cortex affect dopamine metabolism in the rat brain. Brain Res., 860, 77 86. (Pubitemid 30155839)
93. Weinberger, D.R. Lipska, B.K. (1995) Cortical maldevelopment, anti-psychotic drugs, and schizophrenia: a search for common ground. Schizophr. Res., 16, 87 110.
94. Weiner, I. (2003) The 'two-headed' latent inhibition model of schizophrenia: modeling positive and negative symptoms and their treatment. Psychopharmacology, 169, 257 297. (Pubitemid 37264944)
95. Young, A.M., Moran, P.M. Joseph, M.H. (2005) The role of dopamine in conditioning and latent inhibition: what, when, where and how? Neurosci. Biobehav. Rev., 29, 963 976. (Pubitemid 41097395)
96. Zaidel, D.W., Esiri, M.M. Harrison, P.J. (1997) Size, shape, and orientation of neurons in the left and right hippocampus: investigation of normal asymmetries and alterations in schizophrenia. Am. J. Psychiatry, 154, 812 818. (Pubitemid 27230104)
97. Zalc, B. Fields, R.D. (2000) Do action potentials regulate myelination? Neuroscientist, 6, 5 13. (Pubitemid 30140103)
98. Zhuravin, I.A. Bures, J. (1991) Extent of the tetrodotoxin induced blockade examined by pupillary paralysis elicited by intracerebral injection of the drug. Exp. Brain Res., 83, 687 690.