Learning-related Fos-like immunoreactivity in the chick brain: Time-course and co-localization with GABA and parvalbumin

Neuroscience

Volumn 93, Issue 4, 1999, Pages 1515-1524

  Ambalavanar, R ^a   McCabe, B J ^a   Potter, K N ^a   Horn, G ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

c fos; Calbindin D(28k); IMHV; Immediate early genes; Imprinting; Memory

Indexed keywords

4 AMINOBUTYRIC ACID; CALBINDIN; PARVALBUMIN; PROTEIN C FOS;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN; CELL TYPE; CHICKEN; CONTROLLED STUDY; CORPUS STRIATUM; IMMEDIATE EARLY GENE; IMMUNOCYTOCHEMISTRY; IMMUNOREACTIVITY; LEARNING; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TIME; TISSUE DISTRIBUTION;

ANIMALS; ANTIBODIES, MONOCLONAL; BRAIN CHEMISTRY; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; CHICKENS; CONDITIONING (PSYCHOLOGY); GAMMA-AMINOBUTYRIC ACID; IMMEDIATE-EARLY PROTEINS; IMPRINTING (PSYCHOLOGY); MEMORY; NEURONS; PARVALBUMINS; PROTO-ONCOGENE PROTEINS C-FOS; TIME FACTORS;

EID: 0032768255     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(99)00217-1     Document Type: Article

References (87)

1. Abramova A.B., Anokhin K.V. Specific induction of c-fos gene in chick brain during visual imprinting. Zh. Výssh. nerv. Deyat. I. P. Pavlova. 47:1997;766-770.
2. Alkon D.L., Sanchez-Andres J.-V., Ito E., Oka K., Yoshioka T., Collin C. Long-term transformation of an inhibitory into an excitatory GABAergic response. Proc. natn. Acad. Sci. U.S.A. 89:1992;11862-11866.
3. Ambalavanar R., McCabe B.J., Horn G. Distribution of calcium-binding proteins in the intermediate and medial hyperstriatum ventrale (IMHV) of the domestic chick (Gallus gallus domesticus). J. Anat. 183:1993;194-195.
4. Ambalavanar R., McCabe B.J., Horn G. NADPH diaphorase (nitric oxide synthase) in a part of the chick brain involved in imprinting. Brain Res. 644:1994;160-165.
5. Ambalavanar R., van der Zee E.A., Bolhuis J.J., McCabe B.J., Horn G. Co-expression of Fos immunoreactivity in protein kinase (PKCγ)-positive neurones: quantitative analysis of a brain region involved in learning. Brain Res. 606:1993;315-318.
6. Andressen C., Blumcke I., Celio M.R. Calcium-binding proteins: selective markers of nerve cells. Cell Tiss. Res. 271:1993;181-208.
7. Anokhin K.V., Rose S.P.R. Learning-induced increase of immediate early gene messenger RNA in the chick forebrain. Eur. J. Neurosci. 3:1991;162-167.
8. Armstrong R.C., Montminy M.R. Transsynaptic control of gene expression. A. Rev. Neurosci. 16:1993;17-29.
9. Baimbridge K.G., Celio M.R., Rogers J.H. Calcium-binding proteins in the nervous system. Trends Neurosci. 15:1992;303-308.
10. Bateson P., Horn G. Imprinting and recognition memory - a neural net model. Anim. Behav. 48:1994;695-715.
11. Bialy M., Nikolaev E., Beck J., Kaczmarek L. Delayed c-fos expression in sensory cortex following sexual learning in male rats. Molec. Brain Res. 14:1992;352-356.
12. Bliss T.V.P., Errington M.L., Evan G., Hunt S.P. Induction of c-fos-like protein in rat hippocampus following electrical stimulation. J. Physiol., Lond. 398:1988;96P.
13. Bolhuis J.J. Mechanisms of avian imprinting: a review. Biol. Rev. 66:1991;303-345.
14. Bradford C.M., McCabe B.J. Neuronal activity related to memory in the intermediate and medial part of the hyperstriatum (IMHV) of the chick brain. Brain Res. 640:1994;11-16.
15. Bradley P., Horn G., Bateson P. Imprinting: an electron microscopic study of chick hyperstriatum ventrale. Expl Brain Res. 41:1981;115-120.
16. Bradley P.M., Burns B.D., King T.M., Webb A.C. Morphological and electrophysiological properties of neurons in an area of the chick brain involved in learning. Brain Res. 727:1996;125-132.
17. Bradley P.M., Delisle B., Chinnery P.F., Webb A.C. Local circuitry in the IMHV of the domestic chick (Gallus domesticus). Proc. R. Soc. Lond. B. 240:1990;479-492.
18. Braun K., Scheich H., Braun S., Rogers J.H., Heizmann C.W. Parvalbumin-, calretinin-, and calbindin-D28k immunoreactivity and GABA in a forebrain region involved in auditory filial imprinting. Brain Res. 539:1991;31-44.
19. Brennan P.A., Hancock D., Keverne E.B. The expression of the immediate-early genes c-fos, egr-1 and c-jun in the accessory olfactory bulb during the formation of an olfactory memory in mice. Neuroscience. 49:1992;277-284.
20. Brown M.W., Horn G. Learning-related alterations in the visual responsiveness of neurons in a memory system of the chick brain. Eur. J. Neurosci. 6:1994;1479-1490.
21. Bruning G. Localization of NADPH-diaphorase in the brain of the chicken. J. comp. Neurol. 334:1993;192-208.
22. Bruning G., Funk U., Mayer B. Immunocytochemical localization of nitric oxide synthase in the brain of the chicken. NeuroReport. 5:1994;2425-2428.
23. Calamandrei G., Keverne E.B. Differential expression of Fos protein in the brain of female mice dependent on pup sensory cues and maternal experience. Behav. Neurosci. 108:1994;113-120.
24. Celio M.R. Parvalbumin as a marker for fast firing neurons. Neurosci. Lett., Suppl. 18:1984;S32.
25. Celio M.R. GABA neurons contain the calcium-binding protein parvalbumin. Science. 232:1986;995-997.
26. Celio M.R. Calbindin-D28k and parvalbumin in the rat nervous system. Neuroscience. 35:1990;375-475.
27. Cherubini E., Gaiarsa J.L., Ben-Ari Y. GABA: an excitatory transmitter in early postnatal life. Trends Neurosci. 14:1991;515-519.
28. Cipolla-Neto J., Horn G., McCabe B.J. Hemispheric asymmetry and imprinting: the effect of sequential lesions to the hyperstriatum ventrale. Expl Brain Res. 48:1982;22-27.
29. Cotman C.W., Monaghan D.T., Ottersen O.P., Storm-Mathiesen J. Anatomical organisation of excitatory amino acid receptors and their pathways. Trends Neurosci. 10:1987;273-280.
30. Csillag A., Stewart M.G., Curtis E.M. GABA-ergic structures in the chick telencephalon: GABA immunocytochemistry combined with light and electron microscope autoradiography, and Golgi impregnation. Brain Res. 437:1987;283-297.
31. Curtis M., Stewart M.G. Development of γ-aminobutyric acid immunoreactivity in chick hyperstriatum ventrale and cerebellum: light and electron microscopical observations. Devl Brain Res. 30:1986;189-199.
32. DaCosta A.P.C., Broad K.D., Kendrick K.M. Olfactory memory and maternal behaviour-induced changes in c-fos and zif/268 mRNA expression in the sheep brain. Molec. Brain Res. 46:1997;63-76.
33. Davey J.E., Horn G. The development of hemispheric asymmetries in neuronal activity in the domestic chick after visual experience. Behav. Brain Res. 45:1991;81-86.
34. Davies D.C., Taylor D.A., Johnson M.H. The effects of hyperstriatal lesions on one-trial passive- avoidance learning in the chick. J. Neurosci. 8:1988;4662-4666.
35. Dragunow M., Faull R. The use of c-fos as a metabolic marker in neuronal pathway tracing. J. Neurosci. Meth. 29:1989;261-265.
36. Fujiwara K.T., Ashida K., Nishina H., Iba H., Miyajima N., Nishizawa M., Kawai S. The chicken c-fos gene: cloning and nucleotide sequence analysis. J. Virol. 61:1987;4012-4028.
37. Herrera D.G., Robertson H.A. Activation of c-fos in the brain. Prog. Neurobiol. 50:1996;83-107.
38. Horn G. (1985) Memory, Imprinting and the Brain. Oxford University Press, Oxford.
39. Horn G. Neural bases of recognition memory investigated through an analysis of imprinting. Phil. Trans. R. Soc. Lond. B. 329:1990;133-142.
40. Horn G. Visual imprinting and the neural mechanisms of recognition memory. Trends Neurosci. 21:1998;300-306.
41. Horn G., Bradley P., McCabe B.J. Changes in the structure of synapses associated with learning. J. Neurosci. 5:1985;3161-3168.
42. Horn G., McCabe B.J., Bateson P.P.G. An autoradiographic study of the chick brain after imprinting. Brain Res. 168:1979;361-373.
43. Horn G., McCabe B.J., Cipolla-Neto J. Imprinting in the domestic chick: the role of each side of the hyperstriatum ventrale in acquisition and retention. Expl Brain Res. 53:1983;91-98.
44. Hunt S.P., Pini A., Evan G. Induction of c-fos-like protein in spinal cord neurons following sensory stimulation. Nature. 328:1987;632-634.
45. Jeffery K.J., Abraham W.C., Dragunow M., Mason S.E. Induction of Fos-like immunoreactivity and the maintenance of long-term potentiation in the dentate gyrus of unanesthetized rats. Molec. Brain Res. 8:1990;267-274.
46. Johnston A.N., Rogers L.J., Johnston G.A.R. Glutamate and imprinting memory - the role of glutamate receptors in the encoding of imprinting memory. Behav. Brain Res. 54:1993;137-143.
47. Kaczmarek L. Molecular biology of vertebrate learning - is c-fos a new beginning? J. Neurosci. Res. 34:1993;377-381.
48. Konig H., Ponta H., Rahmsdorf U., Buscher M., Schonthal A., Rahmsdorf H.J., Herrlich P. Auto-regulation of Fos - the dyad symmetry element as the major target of repression. Eur. molec. Biol. Org. J. 8:1989;2559-2566.
49. Kubota Y., Jones E.G. Colocalization of 2 calcium-binding proteins in GABA cells of rat piriform cortex. Brain Res. 600:1993;339-344.
50. Kuenzel W. J. and Masson M. (1988) A Stereotaxic Atlas of the Brain of the Chick (Gallus domesticus). The Johns Hopkins University Press, Baltimore.
51. McCabe B. J. (1991) Hemispheric asymmetry of learning-induced changes. In Neural and Behavioural Plasticity. The Use of the Domestic Chick as a Model (ed. Andrew R. J.), pp. 262-276. Oxford University Press, Oxford.
52. McCabe B.J., Cipolla-Neto J., Horn G., Bateson P. Amnesic effects of bilateral lesions in the hyperstriatum ventrale of the chick after imprinting. Expl Brain Res. 48:1982;13-21.
53. McCabe B.J., Davey J.E., Horn G. Impairment of learning by localized injection of an N-methyl-D-aspartate receptor antagonist into the hyperstriatum ventrale of the domestic chick. Behav. Neurosci. 106:1992;947-953.
54. McCabe B.J., Horn G. Learning and memory: regional changes in N-methyl-D-aspartate receptors in the chick brain after imprinting. Proc. natn. Acad. Sci. U.S.A. 85:1988;2849-2853.
55. McCabe B.J., Horn G. Synaptic transmission and recognition memory: time course of changes in N-methyl-D-aspartate receptors after imprinting. Behav. Neurosci. 105:1991;289-294.
56. McCabe B.J., Horn G. Learning-related changes in Fos-like immunoreactivity in the chick forebrain after imprinting. Proc. natn. Acad. Sci. U.S.A. 91:1994;11,417-11,421.
57. McCabe B.J., Horn G., Bateson P.P.G. Effects of restricted lesions of the chick forebrain on the acquisition of filial preferences during imprinting. Brain Res. 205:1981;29-37.
58. Mondadori C., Hengerer B., Ducret T., Borkowski J. Delayed emergence of effects of memory-enhancing drugs - implications for the dynamics of long-term memory. Proc. natn. Acad. Sci. U.S.A. 91:1994;2041-2045.
59. Morgan J.I., Cohen D.R., Hempstead J.L., Curran T. Mapping patterns of c-fos expression in the central nervous system after seizure. Science. 237:1987;192-197.
60. Morgan J.I., Curran T. Stimulus-transcription coupling in the nervous system: involvement of the inducible proto-oncogenes Fos and Jun. A. Rev. Neurosci. 14:1991;421-451.
61. Nicol A.U., Brown M.W., Horn G. Neurophysiological investigations of a recognition memory system for imprinting in the domestic chick. Eur. J. Neurosci. 7:1995;766-776.
62. Nicol A.U., Brown M.W., Horn G. Neural encoding of subject-object distance in a visual recognition system of the domestic chick. Eur. J. Neurosci. 10:1998;34-44.
63. Nikolaev E., Werka T., Kaczmarek L. C-fos protooncogene expression in rat brain after long-term training of two-way active avoidance reaction. Behav. Brain Res. 48:1992;91-94.
64. Nishina H., Sato H., Suzuki T., Sato M., Iba H. Isolation and characterization of fra-2, an additional member of the Fos gene family. Proc. natn. Acad. Sci. U.S.A. 87:1990;3619-3623.
65. Reichling D.B., Kyrozis A., Wang J., MacDermott A.B. Mechanisms of GABA and glycine depolarization-induced calcium transients in rat dorsal horn neurons. J. Physiol., Lond. 476:1994;411-421.
66. Rose S. P. R. (1991) Biochemical mechanisms involved in memory formation in the chick. In Neural and Behavioural Plasticity. The Use of the Domestic Chick as a Model (ed. Andrew R. J.), pp. 277-304. Oxford University Press, Oxford.
67. Rose S.P.R. Cell adhesion molecules, glucocorticoids and long-term memory formation. Trends Neurosci. 18:1995;502-506.
68. Saffen D.W., Cole A.J., Worley P.F., Christy P.A., Ryder K., Baraban J.M. Convulsant-induced increase in transcription factor messenger RNAs in rat brain. Proc. natn. Acad. Sci. U.S.A. 85:1988;7795-7799.
69. Sassonecorsi P., Sisson J.C., Verma I.M. Transcriptional auto-regulation of the proto-oncogene Fos. Nature. 334:1988;314-319.
70. Scheich H. Neural correlates of auditory filial imprinting. J. comp. Physiol. 161:1987;605-609.
71. Sheu F.S., McCabe B.J., Horn G., Routtenberg A. Learning selectively increases protein kinase C substrate phorphorylation in specific regions of the chick brain. Proc. natn. Acad. Sci. U.S.A. 90:1993;2705-2709.
72. Shu S., Ju G., Fan L. The glucose oxidase-DAB-nickel method in peroxidase histochemistry of the nervous system. Neurosci. Lett. 85:1988;169-171.
73. Sluckin W. (1972) Imprinting and Early Learning. Methuen, London.
74. Snedecor G. W. and Cochran W. G. (1989) Statistical Methods. Iowa State University Press, Ames, IA.
75. Solomonia R.O., McCabe B.J., Horn G. Neural cell adhesion molecules, learning and memory. Behav. Neurosci. 112:1998;646-655.
76. Solomonia R.O., McCabe B.J., Jackson A.P., Horn G. Clathrin proteins and recognition memory. Neuroscience. 80:1997;59-67.
77. Sonnenberg J.L., Macgregor-Leon P.F., Curran T., Morgan J.I. Dynamic alterations occur in the levels and composition of transcription factor AP-1 complexes after seizure. Neuron. 3:1989;359-365.
78. Sonnenberg J.L., Mitchelmore C., Macgregor-Leon P.F., Hempstead J., Morgan J.I., et al. Glutamate receptor agonists increase the expression of Fos, Fra and AP-1 DNA binding activity in the mammalian brain. J. Neurosci. Res. 24:1989;72-80.
79. Sonnenberg J.L. III, Rauscher F.J., Morgan J.I., Curran T. Regulation of proenkephalin by Fos and Jun. Science. 246:1989;1622-1625.
80. Swank M.W., Bernstein I.L. C-fos induction in response to a conditioned stimulus after single trial taste-aversion learning. Brain Res. 636:1994;202-208.
81. van der Zee E.A., Bolhuis J.J., Solomonia R.O., Horn G., Luiten P.G.M. Differential distribution of protein kinase C (PKC α, β and γ) isoenzyme immunoreactivity in the chick brain. Brain Res. 676:1995;41-52.
82. Watson A., McCabe B.J., Horn G. Quantitative analysis of the ultrastructural distribution of GABA-like immunoreactivity in the intermediate and medial part of the hyperstriatum ventrale of chick. J. Neurocytol. 20:1991;145-156.
83. Wilson T., Treisman R. Fos C-terminal mutations block down-regulation of c-fos transcription following serum stimulation. Eur. molec. Biol. Org. J. 7:1988;4193-4202.
84. Winer B. J., Brown D. R. and Michels K. M. (1991) Statistical Principles in Experimental Design. McGraw-Hill, New York.
85. Zhu X.O., Brown M.W., McCabe B.J., Aggleton J.P. Effects of the novelty or familiarity of visual stimuli on the expression of the immediate early gene c-fos in rat brain. Neuroscience. 69:1995;821-829.
86. Zhu X.O., McCabe B.J., Aggleton J.P., Brown M.W. Mapping visual recognition memory through expression of the immediate early gene c-fos. NeuroReport. 7:1996;1871-1875.
87. Zhu X.-O., McCabe B.J., Aggleton J.P., Brown M.W. Differential activation of the rat hippocampus and perirhinal cortex by novel visual stimuli and a novel environment. Neurosci. Lett. 229:1997;1-3.