Selective disarrangement of the rostral telencephalic cholinergic system in heterozygous reeler mice

Neuroscience

Volumn 144, Issue 3, 2007, Pages 834-844

  Sigala, S ^a   Zoli, M ^b,c   Palazzolo, F ^a   Faccoli, S ^a   Zanardi, A ^b   Mercuri, N B ^d,e   Spano, P ^a,f  

^a UNIVERSITY OF BRESCIA   (Italy)

^b UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

^c UNIVERSITÉ DE LYON   (France)

^d UNIVERSITY OF ROME TOR VERGATA   (Italy)

^e IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^f IRCCS SAN CAMILLO HOSPITAL   (Italy)

Author keywords

acetylcholinesterase; basal forebrain; choline acetyltransferase; cholinergic neurons; heterozygous reeler mice; reelin

Indexed keywords

ACETYLCHOLINESTERASE; CHOLINE ACETYLTRANSFERASE; REELIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN CELL; BRAIN DEVELOPMENT; CELL MIGRATION; CHOLINERGIC SYSTEM; CONTROLLED STUDY; CORPUS STRIATUM; FEMALE; FOREBRAIN; HETEROZYGOSITY; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NERVE ENDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; TELENCEPHALON;

ACETYLCHOLINE; ANIMALS; BASAL NUCLEUS OF MEYNERT; BIOLOGICAL MARKERS; CELL ADHESION MOLECULES, NEURONAL; CELL DIFFERENTIATION; CELL MOVEMENT; CHOLINE O-ACETYLTRANSFERASE; CHOLINERGIC FIBERS; CORPUS STRIATUM; EXTRACELLULAR MATRIX PROTEINS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HETEROZYGOTE; MALE; MICE; MICE, NEUROLOGIC MUTANTS; NERVE TISSUE PROTEINS; NEURAL PATHWAYS; SERINE ENDOPEPTIDASES; STEM CELLS; TELENCEPHALON;

EID: 33845732649     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2006.10.013     Document Type: Article

References (50)

1. Alcantara S., Ruiz M., D'Arcangelo G., Ezan F., de Lecea L., Curran T., Sotelo C., and Soriano E. Regional and cellular patterns of reelin mRNA expression in the forebrain of the developing and adult mouse. J Neurosci 18 (1998) 7779-7799
2. Aosaki T., Graybiel A.M., and Kimura M. Effect of the nigrostriatal dopamine system on acquired neural responses in the striatum of behaving monkeys. Science 265 (1994) 412-415
3. Ballmaier M., Casamenti F., Zoli M., Pepeu G., and Spano P.F. Selective immunolesioning of cholinergic neurons in nucleus basalis magnocellularis impairs prepulse inhibition of acoustic startle. Neuroscience 108 (2001) 299-305
4. Ballmaier M., Zoli M., Leo G., Agnati L.F., and Spano P.F. Preferential alterations in the mesolimbic dopamine pathway of heterozygous reeler mice: an emerging animal-based model of schizophrenia. Eur J Neurosci 15 (2002) 1197-1205
5. Beaulieu C., and Somogyi P. Enrichment of cholinergic synaptic terminals on GABAergic neurons and coexistence of immunoreactive GABA and choline acetyltransferase in the same synaptic terminals in the striate cortex of the cat. J Comp Neurol 304 (1991) 666-680
6. Benno R.H., Tucker L.W., Joh T.H., and Reis D.J. Quantitative immunocytochemistry of tyrosine hydroxylase in rat brain. I. Development of a computer assisted method using the peroxidase antiperoxidase technique. Brain Res 246 (1982) 225-236
7. Berger-Sweeney J. The cholinergic basal forebrain system during development and its influence on cognitive processes: important questions and potential answers. Neurosci Biobehav Rev 27 (2003) 401-411
8. Brady D.R., Phelps P.E., and Vaughn J.E. Neurogenesis of basal forebrain cholinergic neurons in rat. Dev Brain Res 47 (1989) 81-92
9. Chez M.G., Aimonovitch M., Buchanan T., Mrazek S., and Tremb R.J. Treating autistic spectrum disorders in children: utility of the cholinesterase inhibitor rivastigmine tartrate. J Child Neurol 19 (2004) 165-169
10. Conner J.M., Culberson A., Packowski C., Chiba A.A., and Tuszynski M.H. Lesions of the basal forebrain cholinergic system impair task acquisition and abolish cortical plasticity associated with motor skill learning. Neuron 5 (2003) 819-829
11. Conner J.M., Chiba A.A., and Tuszynski M.H. The basal forebrain cholinergic system is essential for cortical plasticity and functional recovery following brain injury. Neuron 21 (2005) 173-179
12. Costa E., Davis J., Grayson D.R., Guidotti A., Pappas G.D., and Pesold C. Dendritic spine hypoplasticity and downregulation of reelin and GABAergic tone in schizophrenia vulnerability. Neurobiol Dis 8 (2001) 723-742
13. D'Arcangelo G., Miao G.G., and Curran T. Detection of the reelin breakpoint in reeler mice. Brain Res Mol Brain Res 39 (1996) 234-236
14. Erisir A., Levey A.I., and Aoki C. Muscarinic receptor M(2) in cat visual cortex: laminar distribution, relationship to gamma-aminobutyric acidergic neurons, and effect of cingulate lesions. J Comp Neurol 441 (2001) 168-185
15. Fatemi S.H., Earle J.A., and McMenomy T. Reduction in Reelin immunoreactivity in hippocampus of subjects with schizophrenia, bipolar disorder and major depression. Mol Psychiatry 5 (2000) 654-663
16. Fatemi S.H. Reelin glycoprotein in autism and schizophrenia. Int Rev Neurobiol 71 (2005) 179-187
17. Fatemi S.H., Stary J.M., and Egan E.A. Reduced blood levels of reelin as a vulnerability factor in pathophysiology of autistic disorder. Cell Mol Neurobiol 22 (2002) 139-152
18. Franklin K.B.J., and Paxinos G. The mouse brain in stereotaxic coordinates (1998), Academic Press, New York
19. Gross D.S., and Rothfeld J.M. Quantitative immunocytochemistry of hypothalamic and pituitary hormones: validation of an automated, computerized image analysis system. J Histochem Cytochem 33 (1985) 11-20
20. Guidotti A., Auta J., Davis J.M., Di-Giorgi-Gerevini V., Dwivedi Y., Grayson D.R., Impagnatiello F., Pandey G., Pesold C., Sharma R., Uzunov D., and Costa E. Decrease in reelin and glutamic acid decarboxylase67 (GAD67) expression in schizophrenia and bipolar disorder: a postmortem brain study. Arch Gen Psychiatry 57 (2000) 1061-1069
21. Hardan A.Y., and Handen B.L. A retrospective open trial of adjunctive donepezil in children and adolescents with autistic disorder. J Child Adolesc Psychopharmacol 12 (2002) 237-241
22. Hohmann C.F. A morphogenetic role for acetylcholine in mouse cerebral neocortex. Neurosci Biobehav Rev 4 (2003) 351-363
23. Hong S.E., Shugart Y.Y., Huang D.T., Shahwan S.A., Grant P.E., Hourihane J.O., Martin N.D., and Walsh C.A. Autosomal recessive lissencephaly with cerebellar hypoplasia is associated with human RELN mutations. Nat Genet 26 (2000) 93-96
24. Impagnatiello F., Guidotti A.R., Pesold C., Dwivedi Y., Caruncho H., Pisu M.G., Uzunov D.P., Smalheiser N.R., Davis J.M., Pandey G.N., Pappas G.D., Tueting P., Sharma R.P., and Costa E. A decrease of reelin expression as a putative vulnerability factor in schizophrenia. Proc Natl Acad Sci U S A 95 (1998) 15718-15723
25. Liu W.S., Pesold C., Rodriguez M.A., Carboni G., Auta J., Lacor P., Larson J., Condie B.G., Guidotti A., and Costa E. Down-regulation of dendritic spine and glutamic acid decarboxylase 67 expressions in the reelin haploinsufficient heterozygous reeler mouse. Proc Natl Acad Sci U S A 98 (2001) 3477-3482
26. Lysakowski A., Wainer B.H., Bruce G., and Hersh L.B. An atlas of the regional and laminar distribution of choline acetyltransferase immunoreactivity in rat cerebral cortex. Neuroscience 28 (1989) 291-336
27. Mori T., Yuxing Z., Takaki H., Takeuchi M., Iseki K., Hagino S., Kitanaka J., Takemura M., Misawa H., Ikawa M., Okabe M., and Wanaka A. The LIM homeobox gene, L3/Lhx8, is necessary for proper development of basal forebrain cholinergic neurons. Eur J Neurosci 19 (2004) 3129-3141
28. Niederhofer H., Staffen W., and Mair A. Galantamine may be effective in treating autistic disorder. BMJ 325 (2002) 1422-1423
29. Nishikawa S., Goto S., Yamada K., Hamasaki T., and Ushio Y. Lack of reelin causes malpositioning of nigral dopaminergic neurons: evidence from comparison of normal and Reln(rl) mutant mice. J Comp Neurol 461 (2003) 166-173
30. Paxinos G., and Watson C. The rat brain in stereotaxic coordinates (1986), Academic Press, New York
31. Pedrazzi P., Cattaneo L., Valeriani L., Boschi S., Cocchi D., and Zoli M. Hypothalamic neuropeptide Y and galanin in overweight rats fed a cafeteria diet. Peptides 19 (1998) 157-165
32. Perry E., Walker M., Grace J., and Perry R. Acetylcholine in mind: a neurotransmitter correlate to consciousness?. Trends Neurosci 22 (1999) 273-280
33. Pesold C., Impagnatiello F., Pisu M.G., Uzunov D.P., Costa E., Guidotti A., and Caruncho H.J. Reelin is preferentially expressed in neurons synthesizing gamma-aminobutyric acid in cortex and hippocampus of adult rats. Proc Natl Acad Sci U S A 95 (1998) 3221-3226
34. Podhorna J., and Didriksen M. The heterozygous reeler mouse: behavioural phenotype. Behav Brain Res 153 (2004) 43-54
35. Qiu S., Korwek K.M., Pratt-Davis A.R., Peters M., Bergman M.Y., and Weeber E.J. Cognitive disruption and altered hippocampus synaptic function in reelin haploinsufficient mice. Neurobiol Learn Mem 85 (2006) 228-242
36. Reynolds J.N., Hyland B.I., and Wickens J.R. Modulation of an afterhyperpolarization by the substantia nigra induces pauses in the tonic firing of striatal cholinergic interneurons. J Neurosci 24 (2004) 9870-9877
37. Ricceri L., Hohmann C., and Berger-Sweeney J. Early neonatal 192 IgG saporin induces learning impairments and disrupts cortical morphogenesis in rats. Brain Res 954 (2002) 160-172
38. Rice D.S., and Curran T. Role of the reelin signaling pathway in central nervous system development. Annu Rev Neurosci 24 (2001) 1005-1039
39. Rossel M., Loulier K., Feuillet C., Alonso S., and Carroll P. Reelin signaling is necessary for a specific step in the migration of hindbrain efferent neurons. Development 132 (2005) 1175-1185
40. Sarter M., Hasselmo M.E., Bruno J.P., and Givens B. Unraveling the attentional functions of cortical cholinergic inputs: interactions between signal-driven and cognitive modulation of signal detection. Brain Res Brain Res Rev 48 (2005) 98-111
41. Semba K. Multiple output pathways of the basal forebrain: organization, chemical heterogeneity and role in vigilance. Behav Brain Res 115 (2000) 117-141
42. Semba K., and Fibiger H.C. Time of origin of cholinergic neurons in the rat basal forebrain. J Comp Neurol 269 (1988) 87-95
43. Skaar D.A., Shao Y., Haines J.L., Stenger J.E., Jaworski J., Martin E.R., Delong G.R., Moore J.H., McCauley J.L., Sutcliffe J.S., Ashley-Koch A.E., Cuccaro M.L., Folstein S.E., Gilbert J.R., and Pericak-Vance M.A. Analysis of the RELN gene as a genetic risk factor for autism. Mol Psychiatry 10 (2005) 563-571
44. Sternberger L.A., and Sternberger N.H. The unlabeled antibody method: comparison of peroxidase-antiperoxidase with avidin-biotin complex by a new method of quantification. J Histochem Cytochem 34 (1986) 509-605
45. Swerdlow N.R., Braff D.L., Taaid N., and Geyer M.A. Assessing the validity of an animal model of deficient sensorimotor gating in schizophrenic patients. Arch Gen Psychiatry 51 (1994) 139-154
46. Tueting P., Costa E., Dwivedi Y., Guidotti A., Impagnatiello F., Manev R., and Pesold C. The phenotypic characteristics of heterozygous reeler mouse. Neuroreport 10 (1999) 1329-1334
47. Wirths O., Multhaup G., Czech C., Blanchard V., Tremp G., Pradier L., Beyreuther K., and Bayer T.A. Reelin in plaques of beta-amyloid precursor protein and presenilin-1 double-transgenic mice. Neurosci Lett 316 (2001) 145-148
48. Zaborszky L., Pang K., Somogyi J., Nadasdy Z., and Kallo I. The basal forebrain corticopetal system revisited. Ann N Y Acad Sci 877 (1999) 339-367
49. Zoli M., Zini I., Agnati L.F., Guidolin D., Ferraguti F., and Fuxe K. Aspects of neural plasticity in the central nervous system, I. Computer-assisted image analysis method. Neurochem Int 16 (1990) 383-418
50. Zoli M., Guidolin D., and Agnati L.F. Morphometric evaluation of populations of neuronal profiles (cell bodies, dendrites, and nerve terminals) in the central nervous system. Microsc Res Tech 21 (1992) 315-337