DOI: 10.1046/j.1460-9568.2000.00258.x. Differential learning‐stage dependent patterns of c‐Fos protein expression in brain regions during the acquisition and memory consolidation of an operant task in mice

Differential learning‐stage dependent patterns of c‐Fos protein expression in brain regions during the acquisition and memory consolidation of an operant task in mice

10.1046/j.1460-9568.2000.00258.x

Crossref journal-article

Wiley

European Journal of Neuroscience (311)

Abstract

AbstractThe present study analysed the effects of the stage of learning of an appetitive operant conditioning task on the spatial and temporal patterns of c‐Fos protein levels in the brain of BALB/c mice. c‐Fos levels were assessed by immunohistochemistry at either 60, 120 or 180 min after either the first, the second or the fifth daily training session and compared to sham animals. The results show an increase of c‐Fos‐positive nuclei in several subcortical and cortical brain regions, 60‐min post‐acquisition. Because these activations were a function of task mastery, the data indicate that they were specifically related to learning. Following the first acquisition session, significant increases in c‐Fos‐positive neurons were observed in the dorsal hippocampus (CA3), anterior cingulate, occipital and parietal cortices. Following the second daily training session, c‐Fos was highly expressed in some subcortical regions, the hippocampus, the subiculum, the entorhinal, and posterior cingulate areas. Moreover, a significant correlation was found between the progression of performance from day 1 to day 2 and c‐Fos expression on the hippocampal CA1 subfield. Following complete acquisition, no further task‐dependent increases in c‐Fos‐labelled nuclei was observed in any brain region sampled, suggesting that the intervention of c‐Fos‐induced mechanisms in the consolidation process were terminated. The training stage‐dependent changes in regional post‐training c‐Fos expression in the hippocampus and the connected limbic regions suggest that this neuronal network is actively engaged in memory consolidation processes.

Bibliography

BertainaâAnglade, V., Tramu, G., & Destrade, C. (2000). Differential learningâstage dependent patterns of câFos protein expression in brain regions during the acquisition and memory consolidation of an operant task in mice. European Journal of Neuroscience, 12(10), 3803â3812. Portico.

Authors 3

Valérie Bertaina‐Anglade (first)
Gérard Tramu (additional)
Claude Destrade (additional)

References 61 Referenced 69

10.1016/S0006-8993(96)00427-1
10.1016/S0006-8993(97)00651-3
10.1016/0006-8993(91)90890-8
10.1111/j.1460-9568.1991.tb00076.x
10.1146/annurev.ph.55.030193.002145
10.1016/0926-6410(95)90018-7
10.1111/j.1460-9568.1996.tb01198.x
10.1038/23270
10.1016/0306-4522(92)90095-J
10.1016/S0304-3940(97)13395-X
10.1002/(SICI)1097-4695(19971105)33:5<549::AID-NEU5>3.0.CO;2-4
10.1016/S0169-328X(96)00272-0
10.1037/0033-2909.96.3.518
10.1007/978-1-4684-5003-3_18
{'key': 'e_1_2_6_16_1', 'first-page': '389', 'volume-title': 'Investigations Into Time‐Dependent Metabolic Changes During Memory Processing in the Mouse Brain Using (14C) ‐Deoxyglucose and', 'author': 'Destrade C.', 'year': '1992'} / Investigations Into Time‐Dependent Metabolic Changes During Memory Processing in the Mouse Brain Using (14C) ‐Deoxyglucose and by Destrade C. (1992)
10.1016/S0091-6773(73)80113-0
10.1016/0006-8993(88)90993-6
10.1016/0006-8993(86)91239-4
10.1006/nlme.1998.3835
10.1016/0006-8993(82)91201-X
10.1016/0091-3057(83)90280-0
10.1002/cne.903540105
10.1016/S0165-0173(98)00018-6
10.1002/cne.903330212
10.1523/JNEUROSCI.15-07-04786.1995 / J. Neurosci. / Changes in c‐fos mRNA expression in rat brain during odor discrimination learning. differential involvment of hippocampal subfields CA1 and CA3 by Hess U.S. (1995)
10.1523/JNEUROSCI.15-12-07796.1995 / J. Neurosci. / Regional patterns of c‐fos mRNA expression in rat hippocampus following exploration of a novel environment versus performance of a well‐learned discrimination by Hess U.S. (1995)
10.1016/0169-328X(93)90169-P
10.1523/JNEUROSCI.18-17-07027.1998
10.1006/nlme.1997.3799
10.1016/S0091-6773(74)90223-5
10.1016/0304-3940(80)90286-4
10.1016/S0896-6273(00)80396-7
10.1523/JNEUROSCI.16-14-04529.1996
Lehman A.1974.Atlas Stéréotaxique Du Cerveau de la Souris Editions du CNRS Paris.
10.1152/physrev.1990.70.2.453
10.1073/pnas.91.24.11417
10.1002/(SICI)1098-1063(1997)7:4<355::AID-HIPO1>3.0.CO;2-I
10.1016/S0166-4328(05)80018-X
10.1002/(SICI)1097-4695(19990205)38:2<234::AID-NEU6>3.0.CO;2-G
10.1523/JNEUROSCI.18-18-07535.1998
10.1002/(SICI)1098-1063(1998)8:6<608::AID-HIPO3>3.0.CO;2-7
10.1016/S0166-4328(05)80143-3
10.1111/j.1460-9568.1996.tb00733.x
10.1016/0361-9230(94)00254-X
10.1016/0361-9230(93)90299-Q
10.1016/0166-2236(94)90078-7
10.1146/annurev.ne.13.030190.000325
10.1016/0166-2236(91)90027-R
10.1016/0896-6273(90)90106-P
10.1016/0304-3940(88)90346-1
10.1016/0163-1047(91)90279-Y
10.1016/0896-6273(92)90105-M
10.1007/s000180050316
10.1016/S0074-7742(08)60351-7
10.1073/pnas.93.24.13438
10.1007/s000180050315
10.1007/978-1-4684-2979-4_1
10.1006/bbrc.1997.7222
10.1016/0306-4522(92)90004-L
10.1016/0306-4522(95)00320-I
10.1016/S0304-3940(97)00437-0

Dates

Type	When
Created	22 years, 5 months ago (March 6, 2003, 9:27 a.m.)
Deposited	1 year, 10 months ago (Oct. 3, 2023, 4:15 p.m.)
Indexed	1 month, 1 week ago (July 27, 2025, 3:25 a.m.)
Issued	24 years, 11 months ago (Oct. 1, 2000)
Published	24 years, 11 months ago (Oct. 1, 2000)
Published Online	23 years, 8 months ago (Dec. 24, 2001)
Published Print	24 years, 11 months ago (Oct. 1, 2000)

Funders 0

None

BibTeX

@article{Bertaina_Anglade_2000, title={Differential learning‐stage dependent patterns of c‐Fos protein expression in brain regions during the acquisition and memory consolidation of an operant task in mice}, volume={12}, ISSN={1460-9568}, url={http://dx.doi.org/10.1046/j.1460-9568.2000.00258.x}, DOI={10.1046/j.1460-9568.2000.00258.x}, number={10}, journal={European Journal of Neuroscience}, publisher={Wiley}, author={Bertaina‐Anglade, Valérie and Tramu, Gérard and Destrade, Claude}, year={2000}, month=oct, pages={3803–3812} }

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