Environmental enrichment results in higher levels of nerve growth factor mRNA in the rat visual cortex and hippocampus

Behavioural Brain Research

Volumn 93, Issue 1-2, 1998, Pages 83-90

  Torasdotter, Marita ^a   Metsis, Madis ^b   Henriksson, Bengt G ^a   Bengt Winblad, ^a   Mohammed, Abdul H ^a  

^a KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^b Department of Medical Chemistry   (Sweden)

Author keywords

Enriched environment; Hippocampus; Learning; NGF mRNA; Perceptual integration; Plasticity; Visual cortex

Indexed keywords

NERVE GROWTH FACTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ENVIRONMENTAL EXPOSURE; HIPPOCAMPUS; INFORMATION PROCESSING; LEARNING; MALE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; RAT; VISUAL CORTEX;

ANIMALS; ENVIRONMENT; HIPPOCAMPUS; IN SITU HYBRIDIZATION; MALE; NERVE GROWTH FACTORS; NEUROTROPHIN 3; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; VISUAL CORTEX;

EID: 18144440012     PISSN: 01664328     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0166-4328(97)00142-3     Document Type: Article

References (76)

1. Anderson B.J., Li X., Alcantara A.A., Isaacs K.R., Black J.E., Greenough W.T. Glial hypertrophy is associated with synaptogenesis following motor-skill learning, but not with angiogenesis following exercise. GLIA. 11:1994;73-80.
2. Antonini A., Stryker M.P. Development of individual geniculocortical arbors in cat striate cortex and effects of binocular impulse blockade. J Neurosci. 13:1993;3549-3573.
3. Appel S.H. A unifying hypothesis for the cause of amyotrophic lateral sclerosis, Parkinsonism and Alzheimer disease. Ann Neurol. 10:1981;499-505.
4. Arenas E., Persson H. Neurotrophin-3 prevents the death of adult central noradrenergic neurons in vivo. Nature. 367:1994;368-371.
5. Bailey C.H., Kandel E.R. Structural changes accompanying memory storage. Annu Rev Physiol. 55:1993;397-426.
6. Bear M.F., Singer W. Modulation of visual cortical plasticity by acetylcholine and noradrenaline. Nature. 320:1986;172-176.
7. Bear M.F., Kleinschmidt A., Gu Q.A., Singer W. Disruption of experience-dependent synaptic modifications in striate cortex by infusion of an NMDA receptor antagonist. J Neurosci. 10:1990;909-925.
8. Benloucif S., Bennett E.L., Rosenzweig M.R. Norepinephrine and neural plasticity: the effects of xylamine on experience-induced changes in brain weight, memory, and behavior. Neurobiol Learn Memory. 63:1995;33-42.
9. Black J.E., Isaacs K.R., Anderson B.J., Alcantara A.A., Greenough W.T. Learning causes synaptogenesis, whereas motor activity causes angiogenesis, in cerebellar cortex of adult rats. Proc Natl Acad Sci USA. 87:1990;5568-5572.
10. Brenner E., Mirmiran M., Uylings H.B., Van der Gugten J. Impaired growth of the cerebral cortex of rats treated neonatally with 6-hydroxydopamine under different environmental conditions. Neurosci Lett. 42:1983;13-17.
11. Bröcher S., Artola A., Singer W. Agonists of cholinergic and noradrenergic receptors facilitate synergistically the induction of long-term potentiation in slices of rat visual cortex. Brain Res. 573:1992;27-36.
12. Calamandrei G., Alleva E. Neuronal growth factors, neurotrophins and memory deficiency. Behav Brain Res. 66:1995;129-132.
13. Chao M.V., Hempstead B.L. p75 and Trk: a two-receptor system. Trends Neurosci. 18:1995;321-326.
14. Chen K.S., Gage F.H. Somatic gene transfer of NGF to the aged brain: behavioral and morphological amelioration. J Neurosci. 15:1995;2819-2825.
15. Chen K.S., Masliah E., Mallory M., Gage F.H. Synaptic loss in cognitively impaired aged rats is ameliorated by chronic human nerve growth factor infusion. Neuroscience. 68:1995;19-27.
16. Collingridge G.L., Singer W. Excitatory amino acid receptors and synaptic plasticity. Trends Pharmacol Sci. 11:1990;290-296.
17. Diamond M.C., Rosenzweig M.R., Bennett E.L., Lindner B., Lyon L. Effects of environmental enrichment and impoverishment on rat cerebral cortex. J Neurobiol. 3:1972;47-64.
18. Dobrowsky R.T., Jenkins G.M., Hannun Y.A. Neurotrophins induce sphingomyelin hydrolysis. Modulation by co-expression of p75NTR with Trk receptors. J Biol Chem. 270:1995;22135-22142.
19. Ebendal T. NGF in CNS: experimental data and clinical implications. Progr Growth Factor Res. 1:1989;143-159.
20. Ebendal T. Function and evolution in the NGF family and its receptors. J Neurosci Res. 32:1992;461-470.
21. Fiorentini A., Berardi N., Maffei L. Nerve growth factor preserves behavioral visual acuity in monocularly deprived kittens. Vis Neurosci. 12:1995;51-55.
22. Fischer W., Björklund A. Loss of AChE- and NGFr-labeling precedes neuronal death of axotomized septal-diagonal band neurons: reversal by intraventricular NGF infusion. Exp Neurol. 113:1991;93-108.
23. Fischer W., Björklund A., Chen K., Gage F.H. NGF improves spatial memory in aged rodents as a function of age. J Neurosci. 11:1991;1889-1906.
24. Fischer W., Chen K.S., Gage F.H., Björklund A. Progressive decline in spatial learning and integrity of forebrain cholinergic neurons in rats during aging. Neurobiol Aging. 13:1992;9-23.
25. Fox K., Daw N.W. Do NMDA receptors have a critical function in visual cortical plasticity? Trends Neurosci. 16:1993;116-122.
26. Fregnac Y., Shulz D., Thorpe S., Bienenstock E. A cellular analogue of visual cortical plasticity. Nature. 333:1988;367-370.
27. Friedlander M.J., Marin K.A., Wassenhove-McCarthy D. Effects of monocular visual deprivation on geniculocortical innervation of area 18 in cat. J Neurosci. 11:1991;3268-3288.
28. Garofalo L., Ribeiro-da-Silva A., Cuello A.C. Nerve growth factor-induced synaptogenesis and hypertrophy of cortical cholinergic terminals. Proc Natl Acad Sci USA. 89:1992;2639-2643.
29. Globus A., Rosenzweig M.R., Bennett E.L., Diamond M.C. Effects of differential experience on dendritic spine counts in rat cerebral cortex. J Comp Physiol Psychol. 82:1973;175-181.
30. Gnahn H., Hefti F., Heumann R., Schwab M.E., Thoenen H. NGF-mediated increase of choline acetyltransferase (ChAT) in the neonatal rat forebrain: evidence for a physiological role of NGF in the brain? Dev Brain Res. 9:1983;45-52.
31. Greenough W.T., Volkmar F.R. Pattern of dendritic branching in occipital cortex of rats reared in complex environment. Exp Neurol. 40:1973;491-504.
32. Gu Q. Involvement of nerve growth factor in visual cortex plasticity. Rev Neurosci. 6:1995;329-351.
33. Gu Q., Liu Y., Cynader M.S. Nerve growth factor-induced ocular dominance plasticity in adult cat visual cortex. Proc Natl Acad Sci USA. 91:1994;8408-8412.
34. Hebb DO. The Organization of Behaviour. New York: John Wiley and Sons, 1949.
35. Hefti F. Nerve growth factor promotes survival of septal cholinergic neurons after fimbrial transections. J Neurosci. 6:1986;2155-2162.
36. Hefti F., Weiner W.J. Nerve growth factor and Alzheimer's disease. Ann Neurol. 20:1986;275-281.
37. Juraska J.M., Greenough W.T., Elliott C., Mack K.J., Berkowitz R. Plasticity in adult rat visual cortex: an examination of several cell poulations after differential rearing. Behav Neurol Biol. 29:1980;157-167.
38. Kasamatsu T., Pettigrew J.D. Preservation of binocularity after monocular deprivation in the striate cortex of kittens treated with 6-hydroxydopamine. J Comp Neurol. 185:1979;139-161.
39. 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.
40. Kossel A., Löwel S., Bolz J. Relationships between dendritic fields and functional architecture in striate cortex of normal and visually deprived cats. J Neurosci. 15:1995;3913-3926.
41. Kovács I. Gestalten of today: early processing of visual contours and surfaces. Behav Brain Res. 82:1996;1-11.
42. Lärkfors L., Ebendal T., Whittemore S.R., Persson H., Hoffer B., Olson L. Decreased level of nerve growth factor (NGF) and its messenger RNA in the aged rat brain. Brain Res. 427:1987;55-60.
43. Maffei L., Berardi N., Domenici L., Parisi V., Pizzorusso T. Nerve growth factor (NGF) prevents the shift in ocular dominance distribution of visual cortical neurons in monocularly deprived rats. J Neurosci. 12:1992;4651-4662.
44. Martinez-Serrano A., Fischer W., Björklund A. Reversal of age-dependent cognitive impairments and cholinergic neuron atrophy by NGF-secreting neural progenitors grafted to the basal forebrain. Neuron. 15:1995;473-484.
45. Martinez-Serrano A., Fischer W., Söderström S., Ebendal T., Björklund A. Long-term functional recovery from age-induced spatial memory impairments by nerve growth factor gene transfer to the rat basal forebrain. Proc Natl Acad Sci USA. 93:1996;6355-6360.
46. Mervis R.F., Pope D., Lewis R., Dvorak R.M., Williams L.R. Exogenous nerve growth factor reverses age-related structural changes in neocortical neurons in the aging rat. Ann NY Acad Sci. 640:1991;95-101.
47. 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.
48. Mohammed A.K., Jonsson G., Archer T. Selective lesioning of forebrain noradrenaline neurons at birth abolishes the improved maze learning performance induced by rearing in a complex environment. Brain Res. 398:1986;6-10.
49. Mohammed A.H., Henriksson B.G., Söderström S., Ebendal T., Olsson T., Seckl J.R. Environmental influences on the central nervous system and their implications for the aging rat. Behav Brain Res. 57:1993;183-191.
50. Moser M.B., Trommald M., Andersen P. An increase in dendritic spine density on hippocampal CA1 pyramidal cells following spatial learning in adult rats suggests the formation of new synapses. Proc Natl Acad Sci USA. 91:1994;12673-12675.
51. Myhrer T., Utsikt L., Fjelland J., Iversen E.G., Fonnum F. Differential rearing conditions in rats: effects on neurochemistry in neocortical areas and cognitive behaviors. Brain Res Bull. 28:1992;427-434.
52. Pallage V., Orenstein D., Will B. Nerve growth factor and septal grafts: a study of behavioral recovery following partial damage to the septum in rats. Behav Brain Res. 47:1992;1-12.
53. Pallage V., Knusel B., Hefti F., Will B. Functional consequences of a single nerve growth factor administration following septal damage in rats. Eur J Neurosci. 5:1993;669-679.
54. Renner M.J., Rosenzweig M.R. Social interactions among rats housed in groups and enriched conditions. Dev Psychobiol. 19:1986;303-313.
55. Rennert P.D., Heinrich G. Nerve growth factor mRNA in brain: localization by in-situ hybridization. Biochem Biophys Res Commun. 138:1986;813-818.
56. Robbins TW, Everitt BJ. Arousal systems and attention. In: Gazzaniga MS, Bizzi E, editors. The Cognitive Neurosciences. Cambridge: Mass. MIT Press, 1995:703-20.
57. Rosenzweig M.R. Aspects of the search for neural mechanisms of memory. Annu Rev Psychol. 47:1996;1-32.
58. Rosenzweig M.R., Bennett E.L. Psychobiology of plasticity: effects of training and experience on brain and behavior. Behav Brain Res. 78:1996;57-65.
59. Rossor M.N., Iversen L.L., Reynolds G.P., Mountjoy C.Q., Roth M. Neurochemical characteristics of early and late onset types of Alzheimer's disease. Br Med J. 288:1984;961-964.
60. Seiler M., Schwab M.E. Specific retrograde transport of nerve growth factor (NGF) from neocortex to nucleus basalis in the rat. Brain Res. 300:1984;33-39.
61. Singer W. The formation of cooperative cell assemblies in the visual cortex. J Exp Biol. 153:1990;177-197.
62. Singer W. Development and plasticity of cortical processing architectures. Science. 270:1995;758-764.
63. Singer W., Gray C.M. Visual feature integration and the temporal correlation hypothesis. Annu Rev Neurosci. 18:1995;555-586.
64. Sirevaag A.M., Greenough W.T. Differential rearing effects on rat visual cortex synapses. III. Neuronal and glial nuclei, boutons, dendrites, and capillaries. Brain Res. 424:1987;320-332.
65. Sirevaag A.M., Greenough W.T. Plasticity of GFAP-immunorective astrocyte size and number in visual cortex of rats reared in complex environments. Brain Res. 540:1991;273-278.
66. Smith M.A., Makino S., Altemus M., Michelson D., Hong S.K., Kvetnansky R., Post R.M. Stress and antidepressants differentially regulate neurotrophin-3 mRNA expression in the locus coeruleus. Proc Natl Acad Sci USA. 92:1995;8788-8792.
67. Tamura H., Hicks T.P., Hata Y., Tsumoto T., Yamatodani A. Release of glutamate and aspartate from the visual cortex of the cat following activation of afferent pathways. Exp Brain Res. 80:1990;447-455.
68. Thoenen H., Barde Y.A. Physiology of nerve growth factor. Physiol Rev. 60:1980;1284-1335.
69. Torasdotter M., Metsis M., Henriksson B.G., Winblad B., Mohammed A.H. Expression of neurotrophin-3 mRNA in the rat visual cortex and hippocampus is influenced by environmental conditions. Neurosci Lett. 218:1996;107-110.
70. Turner A.M., Greenough W.T. Differential rearing effects on rat visual cortex synapses. I. Synaptic and neuronal density and synapses per neuron. Brain Res. 329:1985;195-203.
71. Verdi J.M., Anderson D.J. Neurotrophins regulate sequential changes in neurotrophin receptor expression by sympathetic neuroblasts. Neuron. 13:1994;1359-1372.
72. Whitehouse P.J., Price D.L., Struble R.G., Clark A.W., Coyle J.T., Delon M.R. Alzheimer's disease and senile dementia: loss of neurons in the basal forebrain. Science. 215:1982;1237-1239.
73. Whittemore S.R., Ebendal T., Lärkfors L., Olson L., Seiger Å., Strömberg I., Persson H. Development and regional expression of β-nerve growth factor messenger RNA and protein in the rat central nervous system. Proc Natl Acad Sci USA. 83:1986;817-821.
74. Whittemore S.R., Friedman P.L., Larhammar D., Persson H., Gonzalez- Carvajal M., Holets V.R. Rat β-nerve growth factor sequence and site of synthesis in the adult hippocampus. J Neurosci Res. 20:1988;403-410.
75. Wiesel T.N. Postnatal development of the visual cortex and the influence of environment. Nature. 299:1982;583-591.
76. Will B., Hefti F. Behavioural and neurochemical effects of chronic intraventricular injections of nerve growth factor in adult rats with fimbria lesions. Behav Brain Res. 17:1985;17-24.