Neonatal functional blockade of the entorhinal cortex results in disruption of accumbal dopaminergic responses observed in latent inhibition paradigm in adult rats

European Journal of Neuroscience

Volumn 25, Issue 8, 2007, Pages 2504-2513

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

^a UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

Conditioned olfactory aversion; In vivo voltammetry; Nucleus accumbens; Recognition memory; Schizophrenia

Indexed keywords

TETRODOTOXIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AVERSIVE BEHAVIOR; BANANA; COMPREHENSION; CONDITIONING; DOPAMINERGIC ACTIVITY; ENTORHINAL CORTEX; FEMALE; IN VIVO STUDY; LATENT INHIBITION; MALE; MICROINJECTION; NONHUMAN; NUCLEUS ACCUMBENS; ODOR; PATHOPHYSIOLOGY; PERINATAL DEVELOPMENT; PERINATAL PERIOD; POTENTIOMETRY; PRIORITY JOURNAL; RAT; SCHIZOPHRENIA;

ANIMALS; ANIMALS, NEWBORN; BEHAVIOR, ANIMAL; CONDITIONING, CLASSICAL; DOPAMINE; ELECTROCHEMISTRY; ENTORHINAL CORTEX; FEMALE; HUMANS; INHIBITION (PSYCHOLOGY); MALE; NUCLEUS ACCUMBENS; POISONS; RANDOM ALLOCATION; RATS; RATS, SPRAGUE-DAWLEY; SCHIZOPHRENIA; TETRODOTOXIN;

EID: 34247282202     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2007.05503.x     Document Type: Article

References (72)

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.
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.
3. Arnold, S.E. (2000) Cellular and molecular neuropathology of the parahippocampal region in schizophrenia. Ann. N.Y. Acad. Sci., 911, 275-292.
4. 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.
5. 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.
6. Besson, C. & Louilot, A. (1995) Asymmetrical involvement of mesolimbic dopaminergic neurons in affective perception. Neuroscience, 68, 963-968.
7. 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.
8. 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.
9. Burglen, F., Marczewski, P., Mitchell, K.J., van der Linden, M., Johnson, M.K., Danion, J.M. & Salamé, P. (2004) Impaired performance in a working memory binding task in patients with schizophrenia. Psychiatry Res., 125, 247-255.
10. 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.
11. Chilton, J.K. (2006) Molecular mechanisms of axon guidance. Dev. Biol., 92, 13-24.
12. Clancy, B., Darlington, R.B. & Finlay, B.L. (2001) Translating developmental time across mammalian species. Neuroscience, 105, 7-17.
13. Danion, J.M., Cuervo, C., Piolino, P., Huron, C., Riutort, M., Peretti, C.S. & Eustache, F. (2005) Conscious recollection in autobiographical memory: an investigation in schizophrenia. Conscious Cogn., 14, 535-547.
14. Danion, J.M., Rizzo, L. & Bruant, A. (1999) Functional mechanisms underlying impaired recognition memory and conscious awareness in patients with schizophrenia. Arch. Gen. Psychiatry, 56, 639-644.
15. Dolorfo, C.L. & Amaral, D.G. (1998) Entorhinal cortex of the rat: topographic organization of the cells of origin of the perforant path projection to the dentate gyrus. J. Comp. Neurol., 398, 25-48.
16. Egorov, A.V., Hamam, B.N., Fransen, E., Hasselmo, M.E. & Alonso, A.A. (2002) Graded persistent activity in entorhinal cortex neurons. Nature, 420, 173-178.
17. 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.
18. Flecknell, P.A. (1987) Laboratory Animal Anaesthesia: An Introduction for Research Workers and Technicians. Academic Press, San Diego, CA, USA.
19. 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.
20. Friston, K.J. (1998) The disconnection hypothesis. Schizophr. Res., 30, 115-125.
21. 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.
22. Garcia, J., Lasiter, P.S., Bermudez-Rattoni, F. & Deems, D.A. (1985) A general theory of aversion learning. Ann. N.Y. Acad. Sci., 443, 8-21.
23. 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.
24. 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. Meth., 39, 231-244.
25. Gray, J.A., Feldon, J., Rawlins, J.N.P., Hemsley, D.R. & Smith, A.D. (1991) The neuropsychology of schizophrenia. Behav. Brain Sci., 14, 1-84.
26. 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.
27. 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.
28. Harrison, P.J. (1999) The neuropathology of schizophrenia. A critical review of the data and their interpretation. Brain, 122, 593-624.
29. Hasselmo, M.E., Fransen, E., Dickson, C. & Alonso, A.A. (2000) Computational modeling of entorhinal cortex. Ann. N.Y. Acad. Sci., 911, 418-446.
30. Huron, C. & Danion, J.M. (2002) Impairment of constructive memory in schizophrenia. Int. Clin. Psychopharmacol., 17, 127-133.
31. Huron, C., Danion, J.M., Giacomoni, F., Grange, D., Robert, P. & Rizzo, L. (1995) Impairment of recognition memory with, but not without, conscious recollection in schizophrenia. Am. J. Psychiatry, 152, 1737-1742.
32. 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.
33. 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.
34. 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.
35. 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.
36. 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.
37. 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.
38. Lewis, D.A. & Levitt, P. (2002) Schizophrenia as a disorder of neurodevelopment. Annu. Rev. Neurosci., 25, 409-432.
39. 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.
40. Louilot, A. & Besson, C. (2000) Specificity of amygdalostriatal interactions in the involvement of mesencephalic dopaminergic neurons in affective perception. Neuroscience, 96, 73-82.
41. Louilot, A., Gonon, F., Buda, M., Simon, H., Le Moal, M. & Pujol, J.F. (1985) Effects of d- and 1-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.
42. 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.
43. Louilot, A. & Le Moal, M. (1994) Lateralized interdependence between limbicotemporal and ventrostriatal dopaminergic transmission. Neuroscience, 59, 495-500.
44. 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.
45. Lubow, R.E. (1989) Latent Inhibition and Conditioned Attention Theory. Cambridge University Press, New York.
46. 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.
47. 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.
48. 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.
49. Murphy, C.A., Pezze, M.A., Feldon, J. & Heidbreder, C. (2000) Differential involvement of dopamine in the shell and core of the nucleus accumbens in the expression of latent inhibition to an aversively conditioned stimulus. Neuroscience, 97, 469-477.
50. 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. N.Y. Acad. Sci., 911, 392-403.
51. 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.
52. Paxinos, G. & Watson, C. (1998) The Rat Brain in Stereotaxic Coordinates, 4th Edn. Academic Press, New York, USA.
53. Pitkaïnen, A., Pikkarainen, M., Nurminen, N. & Ylinen, A. (2000) A reciprocal connection between the amygdala and the hippocampal formation, perirhinal cortex, and postrhinal cortex in rat: a review. Ann. N.Y. Acad. Sci., 911, 369-391.
54. Prasad, K.M., Patel, A.R., Muddasani, S., Sweeney, J. & Keshavan, M.S. (2004) The entorhinal cortex in first-episode psychotic disorders: a structural magnetic resonance imaging study. Am. J. Psychiatry, 161, 1612-1619.
55. 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.
56. Riutort, M., Cuervo, C., Danion, J.M., Peretti, S.C. & Salamé, P. (2003) Reduced levels of specific autobiographical memories in schizophrenia. Psychiatry Res., 117, 35-45.
57. 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.
58. 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.
59. Silver, H., Feldman, P., Bilker, W. & Gur, R.C. (2003) Working memory deficit as a core neuropsychological dysfunction in schizophrenia. Am. J. Psychiatry, 160, 1809-1816.
60. 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.
61. Suzuki, W.A. & Eichenbaum, H. (2000) The neurophysiology of memory. Ann. N. Y. Acad. Sci., 911, 175-191.
62. 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.
63. Tendolkar, I., Ruhrmann, S., Brockhaus, A., Pukrop, R. & Klosterkotter, J. (2002) Remembering or knowing: electrophysiological evidence for an episodic memory deficit in schizophrenia. Psychol. Med., 32, 1261-1271.
64. Totterdell, S. & Meredith, G.E. (1997) Topographical organization of projections from the entorhinal cortex to the striatum of the rat. Neuroscience, 78, 715-729.
65. 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.
66. Weinberger, D.R. & Lipska, B.K. (1995) Cortical maldevelopment, antipsychotic drugs, and schizophrenia: a search for common ground. Schizophr. Res., 16, 87-110.
67. Weiner, I. (2003) The 'two-headed' latent inhibition model of schizophrenia: modeling positive and negative symptoms and their treatment. Psychopharmacology, 169, 257-297.
68. Wikinski, S. (2001) Autobiographic memory: neurobiological substrates. Vertex, 12, 276-282.
69. Witter, M.P., Groenewegen, H.J., Lopes da Silva, F.H. & Lohman, A.H. (1989) Functional organization of the extrinsic and intrinsic circuitry of the parahippocampal region. Prog. Neurobiol., 33, 161-253.
70. Wong, A.H. & Van Tol, H.H. (2003) Schizophrenia: from phenomenology to neurobiology. Neurosci. Biobehav. Rev., 27, 269-306.
71. Young, A.M., Joseph, M.H. & Gray, J.A. (1993) Latent inhibition of conditioned dopamine release in rat nucleus accumbens. Neuroscience, 54, 5-9.
72. 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.