Latent inhibition-related dopaminergic responses in the nucleus accumbens are disrupted following neonatal transient inactivation of the ventral subiculum

Neuropsychopharmacology

Volumn 36, Issue 7, 2011, Pages 1421-1432

  Meyer, Francisca F ^a,b   Louilot, Alain ^a  

^a INSERM   (France)

^b RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

Author keywords

conditioned olfactory aversion; in vivo voltammetry; neonatal functional inactivation; neurodevelopment; nucleus accumbens; schizophrenia

Indexed keywords

TETRODOTOXIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR; CONTROLLED STUDY; DOPAMINERGIC ACTIVITY; FEMALE; HIPPOCAMPUS; HISTOPATHOLOGY; IN VIVO STUDY; LATENT INHIBITION; MALE; NONHUMAN; NUCLEUS ACCUMBENS; POTENTIOMETRY; PRIORITY JOURNAL; RAT; SMELLING; SUBICULUM; VENTRAL SUBICULUM;

ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; BEHAVIOR, ANIMAL; CONDITIONING (PSYCHOLOGY); DOPAMINE; ELECTROCHEMICAL TECHNIQUES; FEMALE; HIPPOCAMPUS; INHIBITION (PSYCHOLOGY); LITHIUM CHLORIDE; NEURAL PATHWAYS; NUCLEUS ACCUMBENS; ODORS; RATS; RATS, SPRAGUE-DAWLEY; RETENTION (PSYCHOLOGY); SODIUM CHANNEL BLOCKERS; TETRODOTOXIN;

EID: 79956038852     PISSN: 0893133X     EISSN: 1740634X     Source Type: Journal    
DOI: 10.1038/npp.2011.26     Document Type: Article

References (98)

1. Ambrogi Lorenzini CG, Baldi E, Bucherelli C, Sacchetti B, Tassoni G (1997). Analysis of mnemonic processing by means of totally reversible neural inactivations. Brain Res Protoc 1: 391-398. (Pubitemid 28281312)
2. Arnold SE (2000). Cellular and molecular neuropathology of the parahippocampal region in schizophrenia. Ann NY Acad Sci 911: 275-292. (Pubitemid 30462088)
3. Arnold SE, Franz BR, Gur RC, Gur RE, Shapiro RM, Moberg PJ et al (1995). Smaller neuron size in schizophrenia in hippo-campal subfields that mediate cortical-hippocampal interactions. Am J Psychiatry 152: 738-748.
4. Arnold SE, Talbot K, Hahn CG (2005). Neurodevelopment, neuroplasticity,and new genes for schizophrenia. Prog Brain Res 147: 319-345.
5. Barres BA, Raff MC (1993). Proliferation of oligodendrocyte precursor cells depends on electrical activity in axons. Nature 361: 258-260. (Pubitemid 23034475)
6. Baruch I, Hemsley DR, Gray JA (1988). Differential performance of acute and chronic schizophrenics in a latent inhibition task. J Nerv Ment Dis 176: 598-606.
7. Besson C, Louilot A (1995). Asymmetrical involvement of mesolimbic dopaminergic neurons in affective perception. Neuroscience 68: 963-968.
8. Blaha CD, Yang CR, Floresco SB, Barr AM, Phillips AG (1997). Stimulation of the ventral subiculum of the hippocampus evokes glutamate receptor-mediated changes in dopamine efflux in the rat nucleus accumbens. Eur J Neurosci 9: 902-911.
9. Brog JS, Salyapongse A, Deutch AY, Zahm DS (1993). The pattern 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: 225-278.
10. Bullmore ET, Frangou S, Murray RM (1997). The dysplastic net hypothesis: an integration of developmental and dysconnectivity theories of schizophrenia. Schizophr Res 28: 143-156. (Pubitemid 28055662)
11. Cano-Cebrian MJ, Zornoza-Sabina T, Guerri C, Polache A, Granero L (2003). Acamprosate blocks the increase in dopamine extracellular levels in nucleus accumbens evoked by chemical stimulation of the ventral hippocampus. Naunyn Schmiedebergs Arch Pharmacol 368: 324-327. (Pubitemid 37372557)
12. Carlsson A, Waters N, Holm-Waters S, Tedroff J, Nilsson M, Carlsson ML (2001). Interactions between monoamines, gluta-mate, and GABA in schizophrenia: new evidence. Annu Rev Pharmacol Toxicol 41: 237-290.
13. Cassaday HJ, Moran PM (2010). Latent inhibition and other salience modulation effects: same neural substrates? In: Lubow RE, Weiner I (eds). Latent Inhibition: Cognition, Neuroscience and Applications to Schizophrenia, 1st edn. Cambridge University Press: Cambridge. pp 342-371.
14. Clancy B, Darlington RB, Finlay BL (2001). Translating developmental time across mammalian species. Neuroscience 105: 7-17. (Pubitemid 32722089)
15. Demerens C, Stankoff B, Logak M, Anglade P, Allinquant B, Couraud F et al (1996). Induction of myelination in the central nervous system by electrical activity. Proc Natl Acad Sci USA 93: 9887-9892. (Pubitemid 26296704)
16. Deutch AY, Cameron DS (1992). Pharmacological characterization of dopamine systems in the nucleus accumbens core and shell. Neuroscience 46: 49-56.
17. 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)
18. Falkai P, Schneider-Axmann T, Honer WG (2000). Entorhinal cortex pre-alpha cell clusters in schizophrenia: quantitative evidence of a developmental abnormality. Biol Psychiatry 47: 937-943. (Pubitemid 30320738)
19. Farber NB, Olney JW (2003). Drugs of abuse that cause developing neurons to commit suicide. Brain Res Dev Brain Res 147: 37-45. (Pubitemid 38114695)
20. Flecknell PA (1987). Laboratory Animal Anaesthesia: An Introduction for Research Workers and Technicians. San Diego, CA: Academic Press.
21. Floresco SB, Todd CL, Grace AA (2001). Glutamatergic afferents from the hippocampus to the nucleus accumbens regulate activity of ventral tegmental area dopamine neurons. J Neurosci 21: 4915-4922. (Pubitemid 32565650)
22. Foucher JR, Vidailhet P, Chanraud S, Gounot D, Grucker D, Pins D et al (2005). Functional integration in schizophrenia: too little or too much? Preliminary Results fMRI Data Neuroimage 26: 374-388.
23. Fricke R, Cowan WM (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.
24. Friston KJ (1998). The disconnection hypothesis. Schizophr Res 30: 115-125. (Pubitemid 28156976)
25. 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.
26. Gal G, Schiller D, Weiner I (2005). Latent inhibition is disrupted by nucleus accumbens shell lesion but is abnormally persistent following entire nucleus accumbens lesion: the neural site controlling the expression and disruption of the stimulus preexposure effect. Behav Brain Res 162: 246-255. (Pubitemid 40828537)
27. Garcia J, Lasiter PS, Bermudez-Rattoni F, Deems DA (1985). A general theory of aversion learning. Ann NY Acad Sci 443: 8-21. (Pubitemid 15074665)
28. Gonon FG, Navarre F, Buda MJ (1984). In vivo monitoring of dopamine release in the rat brain with differential normal pulse voltammetry. Anal Chem 56: 573-575. (Pubitemid 14106520)
29. Gonzalez-Mora JL, 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.
30. Gray NS, Hemsley DR, Gray JA (1992). Abolition of latent inhibition in acute, but not chronic, schizophrenics. Neurol Psychiatry Brain Res 1: 83-89. (Pubitemid 24025553)
31. Gray NS, Pilowsky LS, Gray JA, Kerwin RW (1995). Latent inhibition in drug naive schizophrenics: relationship to duration of illness and dopamine D2 binding using SPET. Schizophr Res 17: 95-107.
32. Groenewegen HJ, Vermeulen-Van der Zee E, te Kortschot A, Witter MP (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)
33. Groenewegen HJ, Wright CI, Beijer AV, Voorn P (1999). Convergence and segregation of ventral striatal inputs and outputs. An NY Acad Sci 877: 49-63. (Pubitemid 29351850)
34. Harrison PJ (1999). The neuropathology of schizophrenia. A critical review of the data and their interpretation. Brain 122: 593-624. (Pubitemid 29158770)
35. Horvitz JC (2000). Mesolimbocortical and nigrostriatal dopamine responses to salient non-reward events. Neuroscience 96: 651-656. (Pubitemid 30155729)
36. Hutchins BI, Kalil K (2008). Differential outgrowth of axons and their branches is regulated by localized calcium transients. J Neurosci 28: 143-153.
37. 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: 351-353.
38. 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)
39. Jennings CA, Cluderay JE, Gartlon J, Cilia J, Lloyd A, Jones DN et al (2006). The effects of ziprasidone on regional c-Fos expression in the rat forebrain. Psychopharmacology (Berl) 184: 13-20. (Pubitemid 43005752)
40. Jongen-Rêlo AL, Kaufmann S, Feldon J (2002). A differential involvement of the shell and core subterritories of the nucleus accumbens of rats in attentional processes. Neuroscience 111: 95-109. (Pubitemid 34310454)
41. Katz LC, Shatz CJ (1996). Synaptic activity and the construction of cortical circuits. Science 274: 1133-1138. (Pubitemid 26389269)
42. Kegeles LS, Abi-Dargham A, Zea-Ponce Y, Rodenhiser-Hill J, Mann JJ, Van Heertum RL et al (2000). Modulation of amphetamine-induced striatal dopamine release by ketamine in humans: implications for schizophrenia. Biol Psychiatry 48: 627-640.
43. Law AJ, Weickert CS, Hyde TM, Kleinman JE, Harrison PJ (2004). Reduced spinophilin but not microtubule-associated protein 2 expression in the hippocampal formation in schizophrenia and mood disorders: molecular evidence for a pathology of dendritic spines. Am J Psychiatry 161: 1848-1855. (Pubitemid 39314679)
44. Legault M, Rompre PP, Wise RA (2000). Chemical stimulation of the ventral hippocampus elevates nucleus accumbens dopamine by activating dopaminergic neurons of the ventral tegmental area. J Neurosci 20: 1635-1642. (Pubitemid 30220442)
45. Legault M, Wise RA (1999). Injections of N-methyl-D-aspartate into the ventral hippocampus increase extracellular dopamine in the ventral tegmental area and nucleus accumbens. Synapse 31: 241-249. (Pubitemid 29070284)
46. Lewis DA, Levitt P (2002). Schizophrenia as a disorder of neurodevelopment. Annu Rev Neurosci 25: 409-432. (Pubitemid 34748023)
47. Louilot A, Choulli MK (1997). Asymmetrical increases in dopamine turn-over in the nucleus accumbens and lack of changes in locomotor responses following unilateral dopaminergic depletions in the entorhinal cortex. Brain Res 778: 150-157. (Pubitemid 28039898)
48. Louilot A, Gonon F, Buda M, Simon H, Le Moal M, Pujol JF (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)
49. Louilot A, Gonzalez-Mora JL, 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.
50. Louilot A, Jeanblanc J, Peterschmitt Y, Meyer F (2010). Parahippocampal region-dopaminergic neuron relationships in latent inhibition. In: Lubow RE, Weiner I (eds). Latent Inhibition: Cognition, Neuroscience and Applications to Schizophrenia. Cambridge: Cambridge University Press. pp 319-341.
51. Louilot A, Le Moal M (1994). Lateralized interdependence between limbicotemporal and ventrostriatal dopaminergic transmission. Neuroscience 59: 495-500. (Pubitemid 24131506)
52. 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)
53. Lubow RE (1989). Latent Inhibition and Conditioned Attention Theory. Cambridge University Press: New York.
54. Lubow RE, 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.
55. Lubow RE, Moore AU (1959). Latent inhibition: the effect of non-reinforced pre-exposure to the conditioned stimulus. J Comp Physiol Psychol 52: 415-419.
56. Martin JH, 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)
57. Marty S, Wehrle R, Sotelo C (2000). Neuronal activity and brain-derived neurotrophic factor regulate the density of inhibitory synapses in organotypic slice cultures of postnatal hippocampus. J Neurosci 20: 8087-8095.
58. Meyer F, Peterschmitt Y, Louilot A (2009). Postnatal functional inactivation of the entorhinal cortex or ventral subiculum has different consequences for latent inhibition-related striatal dopaminergic responses in adult rats. Eur J Neurosci 29: 2035-2048.
59. Mosher HS (1986). The chemistry of tetrodotoxin. Ann NY Acad Sci 479: 32-43. (Pubitemid 17000575)
60. Mulder AB, Hodenpijl MG, Lopes da Silva FH (1998). Electro-physiology of the hippocampal and amygdaloid projections to the nucleus accumbens of the rat: convergence, segregation, and interaction of inputs. J Neurosci 18: 5095-5102. (Pubitemid 28285418)
61. Murphy CA, Pezze MA, 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. (Pubitemid 30320754)
62. Naber PA, Witter MP, Lopes Silva FH (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)
63. 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)
64. O'Neill RD, Lowry JP, Mas M (1998). Monitoring brain chemistry in vivo: voltammetric techniques, sensors, and behavioral applications. Crit Rev Neurobiol 12: 69-127. (Pubitemid 28177264)
65. Paxinos G, Watson C (2009). The Rat Brain in Stereotaxic Coordinates. Compact 6th edn. Academic Press: New-York.
66. 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)
67. 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)
68. 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.
69. Pothuizen HH, Jongen-Rêlo AL, Feldon J, Yee BK (2005). Double dissociation of the effects of selective nucleus accumbens core and shell lesions on impulsive-choice behaviour and salience learning in rats. Eur J Neurosci 10: 2605-2616. (Pubitemid 41759003)
70. Pothuizen HH, Jongen-Rêlo AL, Feldon J, Yee BK (2006). Latent inhibition of conditioned taste aversion is not disrupted, but can be enhanced, by selective nucleus accumbens shell lesions in rats. Neuroscience 137: 1119-1130. (Pubitemid 43133138)
71. Rascle C, Mazas O, Vaiva G, Tournant M, Raybois O, Goudemand M et al (2001). Clinical features of latent inhibition in schizophrenia. Schizophr Res 51: 149-161. (Pubitemid 32772848)
72. Robertson GS, Fibiger HC (1992). Neuroleptics increase c-fos expression in the forebrain: contrasting effects of haloperidol and clozapine. Neuroscience 46: 315-328.
73. Rosenthal R, Rosnow RL (1985). Contrasts Analysis. Focused comparisons in the Analysis of Variance. Cambridge University Press: New York.
74. Rosenthal R, Rosnow RL, Rubin DB (2000). Contrasts and Effect Sizes in Behavioral Research. Cambridge University Press: New York.
75. Rosoklija G, Toomayan G, Ellis SP, Keilp J, Mann JJ, Latov N et al (2000). Structural abnormalities of subicular dendrites in subjects with schizophrenia and mood disorders: preliminary findings. Arch Gen Psychiatry 57: 349-356. (Pubitemid 30202325)
76. Rothfeld JM, Harlan RE, Shivers BD, Pfaff DW (1986). Reversible disruption of lordosis via midbrain infusions of procaine and tetrodotoxin. Pharmacol Biochem Behav 25: 857-863. (Pubitemid 17179905)
77. Sawa A, Snyder SH (2002). Schizophrenia: diverse approaches to a complex disease. Science 296: 692-695. (Pubitemid 34441987)
78. Schlessinger AR, Cowan WM, Gottlieb DI (1975). An autoradio-graphic 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.
79. Singh SC (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: 71-79. (Pubitemid 8160223)
80. Singh SC (1977b). The development of olfactory and hippocampal pathways in the brain of the rat. Anat Embryol (Berl) 151: 183-199. (Pubitemid 8185629)
81. Stryker MP, Harris WA (1986). Binocular impulse blockade prevents the formation of ocular dominance columns in cat visual cortex. J Neurosci 6: 2117-2133. (Pubitemid 16043655)
82. Swerdlow NR, Koob GF (1987). DA, schizophrenia, mania, and depression: toward a unified hypothesis of cortico-striato-pallido-thalamic function. Behav Brain Sci 10: 197-245.
83. Tai CT, Cassaday HJ, Feldon J, Rawlins JN (1995). Both electrolytic, and excitotoxic lesions of nucleus accumbens disrupt latent inhibition of learning in rats. Neurobiol Learn Mem 64: 36-48.
84. Taepavarapruk P, Floresco SB, Phillips AG (2000). Hyperlocomo-tion and increased dopamine efflux in the rat nucleus accumbens evoked by electrical stimulation of the ventral subiculum: role of ionotropic glutamate and dopamine D1 receptors. Psychopharmacology (Berl) 151: 242-251. (Pubitemid 30646428)
85. Totterdell S, Meredith GE (1997). Topographical organization of projections from the entorhinal cortex to the striatum of the rat. Neuroscience 78: 715-729. (Pubitemid 27179654)
86. van Groen T, Lopes da Silva FH (1986). Organization of the reciprocal connections between the subiculum and the entorhinal cortex in the cat: II. An electrophysiological study. J Comp Neurol 251: 111-120. (Pubitemid 16012192)
87. van Groen T, Miettinen P, Kadish I (2003). The entorhinal cortex of the mouse: organization of the projection to the hippocampal formation. Hippocampus 13: 133-149. (Pubitemid 36312926)
88. Voorn P, Vanderschuren LJ, Groenewegen HJ, Robbins TW, Pennartz CM (2004). Putting a spin on the dorsal-ventral divide of the striatum. Trends Neurosci 27: 468-474. (Pubitemid 38951039)
89. Weinberger DR, Lipska BK (1995). Cortical maldevelopment, anti-psychotic drugs, and schizophrenia: a search for common ground. Schizophr Res 16: 87-110.
90. 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)
91. Weiner I (2010). What the brain teaches us about latent inhibition (LI): the neural substrates of the expression and prevention of LI. In: Lubow RE, Weiner I (eds). Latent Inhibition: Cognition, Neuroscience and Applications to Schizophrenia. Cambridge University Press: Cambridge. pp 372-415.
92. Weiner I, Gal G, Feldon J (1999). Disrupted and undisruptable latent inhibition following shell and core lesions. Ann NY Acad Sci 877: 723-727. (Pubitemid 29351900)
93. Weiner I, Gal G, Rawlins JN, Feldon J (1996). Differential involvement of the shell and core subterritories of the nucleus accumbens in latent inhibition and amphetamine-induced activity. Behav Brain Res 81: 123-133. (Pubitemid 26384970)
94. Young AM, Ahier RG, Upton RL, Joseph MH, Gray JA (1998). Increased extracellular dopamine in the nucleus accumbens of the rat during associative learning of neutral stimuli. Neu-roscience 83: 1175-1183. (Pubitemid 28114209)
95. Young AM, Joseph MH, Gray JA (1993). Latent inhibition of conditioned dopamine release in rat nucleus accumbens. Neuroscience 54: 5-9. (Pubitemid 23147083)
96. Young AM, Moran PM, Joseph MH (2005). The role of dopamine in conditioning and latent inhibition: what, when, where and how? Neurosci Biobehav Rev 29: 963-976. (Pubitemid 41097395)
97. Zalc B, Fields RD (2000). Do action potentials regulate myelina-tion? Neuroscientist 6: 5-13.
98. Zhuravin IA, Bures J (1991). Extent of the tetrodotoxin induced blockade examined by pupillary paralysis elicited by intracer-ebral injection of the drug. Exp Brain Res 83: 687-690.