NGF induces appearance of adult-like response to spatial novelty in 18-day male mice

Behavioural Brain Research

Volumn 136, Issue 1, 2002, Pages 289-298

  Calamandrei, Gemma ^a   Valanzano, Angela ^a   Ricceri, Laura ^a  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

Author keywords

Choline acetyl transferase; Mice; Nerve growth factor; Novelty; Sex differences; Spatial cognition

Indexed keywords

CHOLINE ACETYLTRANSFERASE; NERVE GROWTH FACTOR;

ANIMAL BEHAVIOR; ARTICLE; CONTROLLED STUDY; DEVELOPMENT; DISCRIMINATION LEARNING; DRUG EFFECT; ENZYME ACTIVITY; FEMALE; HABITUATION; HIPPOCAMPUS; LOCOMOTION; MALE; MOUSE; NEOCORTEX; NEWBORN; NONHUMAN; OPEN FIELD TEST; PERINATAL PERIOD; PRIORITY JOURNAL;

ANIMALS; BEHAVIOR, ANIMAL; CHOLINE O-ACETYLTRANSFERASE; FEMALE; FORM PERCEPTION; HABITUATION, PSYCHOPHYSIOLOGIC; INJECTIONS, INTRAVENTRICULAR; MALE; MICE; NERVE GROWTH FACTORS; PARASYMPATHETIC NERVOUS SYSTEM; PROSENCEPHALON; SEX CHARACTERISTICS; SPACE PERCEPTION;

EID: 0037126136     PISSN: 01664328     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0166-4328(02)00140-7     Document Type: Article

References (60)

1. Alleva E., Bignami G. Development of mouse activity, stimulus reactivity, habituation, and response to amphetamine and scopolamine. Physiol. Behav. 34:1985;519-523.
2. Alleva E., Aloe L., Laviola G. Pretreatment of young mice with nerve growth factor enhances scopolamine-induced hyperactivity. Brain Res. 393:1986;278-281.
3. Arters J., Hohmann C.F., Mills J., Olaghere O., Berger-Sweeney J. Sexually dimorphic responses to neonatal basal forebrain lesions in mice: I. Behavior and neurochemistry. J. Neurobiol. 37:1998;582-594.
4. Auburger G., Heumann R., Hellweg R., Korsching S., Thoenen H. Developmental changes of nerve growth factor and its mRNA in the rat hippocampus: comparison with choline acetyltransferase. Dev. Biol. 120:1987;322-328.
5. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:1976;248-254.
6. Brandner C., Vantini G., Schenk F. Postnatal intracerebroventricular administrations of NGF alter spatial memory in adulthood. Behav. Brain Res. 111:2000;165-173.
7. Brandner C., Vantini G., Schenk F. Enhanced visuospatial memory following intracerebroventricular administration of nerve growth factor. Neurobiol. Learn. Mem. 73:2000;49-67.
8. Berger-Sweeney J., Arnold A., Gabeau D., Mills J. Sex differences in learning and memory in mice: effects of sequence of testing and cholinergic blockade. Behav. Neurosci. 109:1995;859-873.
9. Calamandrei G., Alleva E. Neuronal growth factors, neurotrophins and memory deficiency. Behav. Brain Res. 66:1995;129-132.
10. Calamandrei G., Valanzano A. Age-dependent effects of NGF and scopolamine on suckling behavior of neonatal mice. Pharmacol. Biochem. Behav. 49:1994;1043-1048.
11. Calamandrei G., Ricceri L., Valanzano A. Systemic administration of anti-NGF antibodies to neonatal mice impairs 24-h retention of an inhibitory avoidance task while increasing ChAT immunoreactivity in the medial septum. Behav. Brain Res. 78:1996;81-91.
12. Calamandrei G., Valanzano A., Alleva E. NGF and cholinergic control of behavior: anticipation and enhancement of scopolamine effects in neonatal mice. Dev. Brain Res. 61:1991;237-241.
13. Calamandrei G., Alleva E., Cirulli F., Queyras A., Volterra V., Capirci O., Vicari S., Giannotti A., Turrini P., Aloe L. Serum NGF levels in children and adolescents with either Williams syndrome or Down syndrome. Dev. Med. Child Neurol. 42:2000;746-750.
14. Cirulli F., Shooter E.M., Levine S. Developmental expression of the NGF receptor p140trk in the septohippocampal system of the rat: a quantitative analysis. Int. J. Dev. Neurosci. 15:1997;901-909.
15. Dunnett S.B., Everitt B.J., Robbins T.W. The basal forebrain-cortical cholinergic system: interpreting the functional consequences of excitotoxic lesions. Trends Neurosci. 14:1991;494-501.
16. Everitt B.J., Robbins T.W. Central cholinergic systems and cognition. Annu. Rev. Psychol. 48:1997;649-684.
17. Fischer W., Bjorklund A., Chen K., Gage F.H. NGF improves spatial memory in aged rodents as a function of age. J. Neurosci. 11:1991;1889-1906.
18. Fonnum F. A rapid radiochemical method for the determination of choline acetyltransferase. J. Neurochem. 24:1975;407-409.
19. Gibbs R.B. Impairment of basal forebrain cholinergic neurons associated with aging and long-term loss of ovarian function. Exp. Neurol. 151:1998;289-302.
20. Gustilo M.C., Markowska A.L., Breckler S.J., Fleischman C.A., Price D.L., Koliatsos V.E. Evidence that nerve growth factor influences recent memory through structural changes in septohippocampal cholinergic neurons. J. Comp. Neurol. 405:1999;491-507.
21. Johnston M.V., Rutkowski J.L., Wainer B.H., Long J.B., Mobley W.C. NGF effects on developing forebrain cholinergic neurons are regionally specific. Neurochem. Res. 12:1987;985-994.
22. Kornack D.R., Lu B., Black I.B. Sexually dimorphic expression of the NGF receptor gene in the developing rat brain. Brain. Res. 542:1991;171-174.
23. Korsching S., Auburger G., Heumann R., Scott J., Thoenen H. Levels of nerve growth factor and its mRNA in the central nervous system of the rat correlate with cholinergic innervation. Embo. J. 4:1985;1389-1393.
24. Lappalainen R., Lindholm D., Riikonen R. Low levels of nerve growth factor in cerebrospinal fluid of children with Rett syndrome. J. Child Neurol. 11:1996;296-300.
25. Levi-Montalcini R. The saga of the nerve growth factor. Neuroreport. 9:1998;R71-R83.
26. Li Y., Holtzman D.M., Kromer L.F., Kaplan D.R., Chua-Couzens J., Clary D.O., Knusel B., Mobley W.C. Regulation of TrkA and ChAT expression in developing rat basal forebrain: evidence that both exogenous and endogenous NGF regulate differentiation of cholinergic neurons. J. Neurosci. 15:1995;2888-2905.
27. Lipani J.D., Bhattacharjee M.B., Corey D.M., Lee D.A. Reduced nerve growth factor in Rett syndrome postmortem brain tissue. J. Neuropathol. Exp. Neurol. 59:2000;889-895.
28. Loy R., Sheldon R.A. Sexually dimorphic development of cholinergic enzymes in the rat septohippocampal system. Brain Res. 431:1987;156-160.
29. Luine V.N., Renner K.J., Heady S., Jones K.J. Age and sex-dependent decreases in ChAT in basal forebrain nuclei. Neurobiol. Aging. 7:1986;193-198.
30. Markowska A.L., Koliatsos V.E., Breckler S.J., Price D.L., Olton D.S. Human nerve growth factor improves spatial memory in aged but not in young rats. J. Neurosci. 14:1994;4815-4824.
31. Miller J.C. Sex differences in dopaminergic and cholinergic activity and function in the nigro-striatal system of the rat. Psychoneuroendocrinology. 8:1983;225-236.
32. Milner T.A., Loy R., Amaral D.G. An anatomical study of the development of the septo-hippocampal projection in the rat. Brain Res. 284:1983;343-371.
33. Mobley W.C., Rutkowski J.L., Tennekoon G.I., Buchanan K., Johnston M.V. Choline acetyltransferase activity in striatum of neonatal rats increased by nerve growth factor. Science. 229:1985;284-287.
34. Mobley W.C., Rutkowski J.L., Tennekoon G.I., Gemski J., Buchanan K., Johnston M.V. Nerve growth factor increases choline acetyltransferase activity in developing basal forebrain neurons. Brain Res. 387:1986;53-62.
35. Montoya D.A.C., White A.M., Williams C.L., Blusztajn J.K., Meck W.H., Swartzwelder H.S. Prenatal choline exposure alters hippocampal responsiveness to cholinergic stimulation in adulthood. Dev. Brain Res. 123:2000;25-32.
36. Perry T., Hodges H., Gray J.A. Behavioural, histological and immunocytochemical consequences following 192 IgG-saporin immunolesions of the basal forebrain cholinergic system. Brain Res. Bull. 54:2001;29-48.
37. Pizzorusso T., Fagiolini M., Gianfranceschi L., Porciatti V., Maffei L. Role of neurotrophins in the development and plasticity of the visual system: experiments on dark rearing. Int. J. Psychophysiol. 35:2000;189-196.
38. Poucet B. Object exploration, habituation, and response to a spatial change in rats following septal or medial frontal cortical damage. Behav. Neurosci. 103:1989;1009-1016.
39. Rhodes M.E., Rubin R.T. Functional sex differences ('sexual diergism') of central nervous system cholinergic systems, vasopressin, and hypothalamic-pituitary-adrenal axis activity in mammals: a selective review. Brain Res. Brain Res. Rev. 30:1999;135-152.
40. Ricceri L., Berger-Sweeney J. Postnatal choline supplementation in preweanling mice: sexually dimorphic behavioral and neurochemical effects. Behav. Neurosci. 112:1998;1387-1392.
41. Ricceri L., Alleva E., Calamandrei G. Impairment of passive avoidance learning following repeated administrations of antibodies against nerve growth factor in neonatal mice. Neuroreport. 5:1994;1401-1404.
42. Ricceri L., Colozza C., Calamandrei G. Ontogeny of spatial discrimination in mice: a longitudinal analysis in the modified open-field with objects. Dev. Psychobiol. 37:2000;109-118.
43. Ricceri L., Alleva E., Chiarotti F., Calamandrei G. Nerve growth factor affects passive avoidance learning and retention in developing mice. Brain Res. Bull. 39:1996;219-226.
44. Ricceri L., Ewusi A., Calamandrei G., Berger-Sweeney J. Sexually dimorphic effects of anti-NGF treatment in neonatal rats. Dev. Brain Res. 101:1997;273-276.
45. Ricceri L., Usiello A., Calamandrei G., Frick K., Berger-Sweeney J. Neonatal 192 IgG saporin lesions of the medial septal area and nucleus basalis magnocellularis differently affect response to spatial novelty. 28th Annual Meeting of Society for Neuroscience. 1:1998;178 Los Angeles, CA USA.
46. Ricceri L., Usiello A., Valanzano A., Calamandrei G., Frick K., Berger-Sweeney J. Neonatal 192 IgG-saporin lesions of basal forebrain cholinergic neurons selectively impair response to spatial novelty in adult rats. Behav. Neurosci. 113:1999;1204-1215.
47. Riikonen R.S., Soderstrom S., Vanhala R., Ebendal T., Lindholm D.B. West syndrome: cerebrospinal fluid nerve growth factor and effect of ACTH. Pediatr. Neurol. 17:1997;224-229.
48. Sargolini F., Roullet P., Oliverio A., Mele A. Effects of lesions to the glutamatergic afferents to the nucleus accumbens in the modulation of reactivity to spatial and non-spatial novelty in mice. Neuroscience. 93:1999;855-867.
49. Save E., Poucet B., Foreman N., Buhot M.C. Object exploration and reactions to spatial and nonspatial changes in hooded rats following damage to parietal cortex or hippocampal formation. Behav. Neurosci. 106:1992;447-456.
50. Semba K., Fibiger H.C. Time of origin of cholinergic neurons in the rat basal forebrain. J. Comp. Neurol. 269:1988;87-95.
51. Smolen A., Smolen T.N., Han P.C., Collins A.C. Sex differences in the recovery of brain acetylcholinesterase activity following a single exposure to DFP. Pharmacol. Biochem. Behav. 26:1987;813-820.
52. Suzaki I., Hara T., Tanaka C., Dejima S., Takeshita K. Elevated nerve growth factor levels in cerebrospinal fluid associated with progressive cortical atrophy. Neuropediatrics. 28:1997;268-271.
53. Thinus-Blanc C., Save E., Rossi-Arnaud C., Tozzi A., Ammassari-Teule M. The differences shown by C57BL/6 and DBA/2 inbred mice in detecting spatial novelty are subserved by a different hippocampal and parietal cortex interplay. Behav. Brain Res. 80:1996;33-40.
54. Usiello A., Sargolini F., Roullet P., Ammassari-Teule M., Passino E., Oliverio A., Mele A. N-methyl-D-aspartate receptors in the nucleus accumbens are involved in detection of spatial novelty in mice. Psychopharmacology (Berl). 137:1998;175-183.
55. Vantini G., Schiavo N., Di Martino A., Polato P., Triban C., Callegaro L., Toffano G., Leon A. Evidence for a physiological role of nerve growth factor in the central nervous system of neonatal rats. Neuron. 3:1989;267-273.
56. Whittemore S.R., Ebendal T., Larkfors L., Olson L., Seiger A., Stromberg I., Persson H. Development and regional expression of beta nerve growth factor messenger RNA and protein in the rat central nervous system. Proc. Natl. Acad. Sci. USA. 83:1986;817-821.
57. Whittemore S.R., Seiger A. The expression, localization and functional significance of beta-nerve growth factor in the central nervous system. Brain Res. 434:1987;439-464.
58. Wilcox R.G. New statistical procedures for the social sciences. 1987;Erlbaum, Hillsdale, NJ.
59. Williams C.L., Meck W.H., Heyer D.D., Loy R. Hypertrophy of basal forebrain neurons and enhanced visuospatial memory in perinatally choline-supplemented rats. Brain Res. 794:1998;225-238.
60. Zorrilla E.P. Multiparous species present problems (and possibilities) to developmentalists. Dev. Psychobiol. 30:1997;141-150.