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Anterior thalamic lesions produce chronic and profuse transcriptional deregulation in retrosplenial cortex: a model of retrosplenial hypoactivity and covert pathology

Published online by Cambridge University Press:  11 March 2008

G.L. Poirier ,
K.L. Shires ,
D. Sugden ,
E. Amin ,
K.L. Thomas ,
D.A. Carter  and
J.P. Aggleton
G.L. Poirier*
Affiliation:
School of Psychology, Cardiff University, Cardiff, UK
K.L. Shires*
Affiliation:
School of Psychology, Cardiff University, Cardiff, UK School of Biosciences, Cardiff University, Cardiff, UK Division of Reproduction and Endocrinology, School of Biomedical and Health Sciences, King's College, London, UK
D. Sugden
Affiliation:
Division of Reproduction and Endocrinology, School of Biomedical and Health Sciences, King's College, London, UK
E. Amin
Affiliation:
School of Psychology, Cardiff University, Cardiff, UK
K.L. Thomas
Affiliation:
School of Biosciences, Cardiff University, Cardiff, UK
D.A. Carter
Affiliation:
School of Biosciences, Cardiff University, Cardiff, UK
J.P. Aggleton
Affiliation:
School of Psychology, Cardiff University, Cardiff, UK
*
Correspondence should be addressed to: Guillaume Poirier, School of Psychology, Cardiff University, 70 Park Place, Cardiff, UK, CF10 3AT tel: 44 (0) 29 2087 5301 fax: 44 (0) 29 2087 4858 email: [email protected]
Kate Shires, Centre for Cognitive and Neural Systems, Dept of Neuroscience, University of Edinburgh, 1 George Square, Edinburgh, UK, EH8 9JZ tel: +44 131 650 4571 fax: +44 131 651 1835 email: [email protected]
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Abstract

Anterior thalamic lesions are thought to produce ‘covert pathology’ in retrosplenial cortex, but the causes are unknown. Using microarray analyses we tested the hypothesis that thalamic damage causes a chronic, hypofunction of metabolic and plasticity-related pathways (Experiment 1). Rats with unilateral, anterior thalamic lesions were exposed to a novel environment for 20 min, and granular retrosplenial tissue sampled from both hemispheres 30 min, 2 hours and 8 hours later. Complementary statistical approaches (analyses of variance, predictive patterning and gene set-enrichment analysis) revealed pervasive gene expression differences between retrosplenial cortex ipsilateral to the thalamic lesion and contralateral to the lesion. Selected gene differences were validated by QPCR, immunohistochemistry (Experiment 1) and in situ hybridization (Experiment 2). Following thalamic lesions, the retrosplenial cortex undergoes profuse cellular transcriptome changes including lower relative levels of specific mRNAs that are involved in energy metabolism and neuronal plasticity. These changes in functional gene expression might be driven largely by decreases in the expression of genes encoding transcription factors including brd8, c-fos, fra-2, klf5, nfix, nr4a1, smad3, smarcc2 and zfp9, with far fewer (nfat5, neuroD1 and RXRγ) showing increases. These findings have implications for conditions such as diencephalic amnesia and Alzheimer's disease in which both anterior thalamic pathology and retrosplenial cortex hypometabolism are prominent.

Keywords

Alzheimer's diseasegenemicroarraypathology
Type
Original Articles
Information
Thalamus & Related Systems , Volume 4 , Issue 1 , March 2008 , pp. 59 - 77
Copyright
Copyright © Cambridge University Press 2008

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References

REFERENCES

Aggleton, J.P. and Sahgal, A. (1993) The contribution of the anterior thalamic nuclei to anterograde amnesia. Neuropsychologia 31, 1001–1019.CrossRefGoogle ScholarPubMed
Aggleton, J.P. and Brown, M.W. (1999) Episodic memory, amnesia, and the hippocampal-anterior thalamic axis. Behavioral and Brain Sciences 22, 425–444.CrossRefGoogle ScholarPubMed
Albasser, M.M., Poirier, G.L., Warburton, E.C., Aggleton, J.P. (2007) Hippocampal lesions halve immediate-early gene protein counts in retrosplenial cortex: distal dysfunctions in a spatial memory system. European Journal of Neuroscience 26, 1254–1266.CrossRefGoogle Scholar
Allen, P.B., Hvalby, O., Jensen, V., Errington, M.L., Ramsay, M., Chaudhry, F.A. et al. (2000) Protein phosphatase-1 regulation in the induction of long-term potentiation: Heterogeneous molecular mechanisms. Journal of Neuroscience 20, 3537–3543.CrossRefGoogle ScholarPubMed
Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J., Zhang, Z., Miller, W. et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25, 3389–3402.CrossRefGoogle ScholarPubMed
Archer, J.S., Abbott, D.F., Waites, A.B. and Jackson, G.D. (2003) fMRI “deactivation” of the posterior cingulate during generalized spike and wave. NeuroImage 20, 1915–1922.CrossRefGoogle ScholarPubMed
Aupée, A.M., Desgranges, B., Eustache, F., Lalevée, C., de la Sayette, V., Viader, F. et al. (2001) Voxel-based mapping of brain hypometabolism in permanent amnesia with PET. NeuroImage 13, 1164–1173.CrossRefGoogle ScholarPubMed
Bachevalier, J. and Meunier, M. (1996) Cerebral ischemia: are the memory deficits associated with hippocampal cell loss? Hippocampus 6, 553–560.3.0.CO;2-J>CrossRefGoogle ScholarPubMed
Baron, J.C., Chételat, G., Desgranges, B., Perchey, G., Landeau, B., de la Sayette, V. et al. (2001) In vivo mapping of gray matter loss with voxel-based morphometry in mild Alzheimer's disease. Neuroimage 14, 298–309.CrossRefGoogle ScholarPubMed
Bedford, F.K., Kittler, J.T., Muller, E., Thomas, P., Uren, J.M., Merlo, D. et al. (2001) GABAA receptor cell surface number and subunit stability are regulated by the ubiquitin-like protein Plic-1. Nature Neuroscience 4, 908–916.CrossRefGoogle ScholarPubMed
Benjamini, Y. and Hochberg, Y. (1995) Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society: Series B 57, 289–300.Google Scholar
Braak, H. and Braak, E. (1991a) Alzheimer's disease affects limbic nuclei of the thalamus. Acta Neuropathoogica 81, 261–268.CrossRefGoogle ScholarPubMed
Braak, H. and Braak, E. (1991b) Neuropathological stageing of Alzheimer-related changes. Acta Neuropathoogica 82, 239–259.Google ScholarPubMed
Brackmann, M., Zhao, C., Kuhl, D., Manahan-Vaughan, D. and Braunewell, K.-H. (2004) MGluRs regulate the expression of neuronal calcium sensor proteins NCS-1 and VILIP-1 and the immediate early gene arg3.1/arc in the hippocampus in vivo. Biochemical and Biophysical Research Communications 322, 1073–1079.CrossRefGoogle ScholarPubMed
Brandon, E.P., Zhuo, M., Huang, Y., Qi, M., Gerhold, K.A., Burton, K.A. et al. (1995) Hippocampal long-term depression and depotentiation are defective in mice carrying a targeted disruption of the gene encoding the RIß subunit of cAMP-dependent protein kinase. Proceedings of the National Academy of Sciences of the United States of America 92, 8851–8855.CrossRefGoogle Scholar
Brenner, E., Kondziella, D., Haberg, A. and Sonnewald, U. (2005) Impaired glutamine metabolism in NMDA receptor hypofunction induced by MK801. Journal of Neurochemistry 94, 1594–1603.CrossRefGoogle ScholarPubMed
Buytaert, K.A., Kline, A.E., Montanez, S., Likler, E., Millar, C.J. and Hernandez, T.D. (2001) The temporal patterns of c-Fos and basic fibroblast growth factor expression following a unilateral anteromedial cortex lesion. Brain Research 894, 121–130.Google ScholarPubMed
Carpenedo, R., Meli, E., Peruginelli, F., Pellegrini-Giampietro, D.E. and Moroni, F. (2002) Kynurenine 3-mono-oxygenase inhibitors attenuate post-ischemic neuronal death in organotypic hippocampal slice cultures. Journal of Neurochemistry 82, 1465–1471.CrossRefGoogle ScholarPubMed
Cavallaro, S., D'Agata, V., Manickam, P., Dufour, F. and Alkon, D.L. (2002) Memory-specific temporal profiles of gene expression in the hippocampus. Proceedings of the National Academy of Sciences of the United States of America 99, 16279–16284.CrossRefGoogle ScholarPubMed
Chételat, G., Desgranges, B., De La Sayette, V., Viader, F., Eustache, F. and Baron, J.C. (2002) Mapping gray matter loss with voxel-based morphometry in mild cognitive impairment. Neuroreport 13, 1939–1943.CrossRefGoogle ScholarPubMed
Chételat, G., Desgranges, B., de la Sayette, V., Viader, F., Berkouk, K., Landeau, B. et al. (2003) Dissociating atrophy and hypometabolism impact on episodic memory in mild cognitive impairment. Brain 126, 1955–1967.CrossRefGoogle ScholarPubMed
Chiang, M.-Y., Misner, D., Kempermann, G., Schikorski, T., Giguere, V., Sucov, H.M. et al. (1998) An essential role for retinoid receptors RARβ and RXRγ in long-term potentiation and depression. Neuron 21, 1353–1361.CrossRefGoogle ScholarPubMed
Chomczynski, P. and Sacchi, N. (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Analytical Biochemistry 162, 156–159.Google ScholarPubMed
Daw, M.I., Ashby, M.C. and Isaac, J.T.R. (2007) Coordinated developmental recruitment of latent fast spiking interneurons in layer IV barrel cortex. Nature Neuroscience 10, 453–461.CrossRefGoogle ScholarPubMed
Desgranges, B., Baron, J.-C., Lalevée, C., Giffard, B., Viader, F., de la Sayette, V. et al. (2002) The neural substrates of episodic memory impairment in Alzheimer's disease as revealed by FDG-PET: relationship to degree of deterioration. Brain 125, 1116–1124.CrossRefGoogle ScholarPubMed
de Quervain, D.J.F., Poirier, R., Wollmer, M.A., Grimaldi, L.M.E., Tsolaki, M., Streffer, J.R., Hock, C., Nitsch, R.M., Mohajeri, M.H., Papassotiropoulos, A. (2004) Glucocorticoid-related genetic susceptibility for Alzheimer's disease. Human Molecular Genetics 13, 47–52.CrossRefGoogle ScholarPubMed
Drzezga, A., Lautenschlager, N., Siebner, H., Riemenschneider, M., Willoch, F., Minoshima, S. et al. (2003) Cerebral metabolic changes accompanying conversion of mild cognitive impairment into Alzheimer's disease: a PET follow-up study. European Journal of Nuclear Medicine and Molecular Imaging 30, 1104–1113.Google ScholarPubMed
Erhardt, S. and Engberg, G. (2002) Increased phasic activity of dopaminergic neurones in the rat ventral tegmental area following pharmacologically elevated levels of endogenous kynurenic acid. Acta Physiologica Scandinavica 175, 45–53.Google ScholarPubMed
Fazio, F., Perani, D., Gilardi, M.C., Colombo, F., Cappa, S.F., Vallar, G. et al. (1992) Metabolic impairment in human amnesia: a PET study of memory networks. Journal of Cerebral Blood Flow and Metabolism 12, 353–358.CrossRefGoogle ScholarPubMed
Figiel, M. and Engele, J. (2000) Pituitary adenylate cyclase-activating polypeptide (PACAP), a neuron-derived peptide regulating glial glutamate transport and metabolism. Journal of Neuroscience 20, 3596–3605.CrossRefGoogle ScholarPubMed
Garden, D.L.F., Warburton, E.C., Barker, G.R.I., Aggleton, J.P., Brown, M.W. and Bashir, Z.I. (2006) A role for anterior thalamic nuclei in determining synaptic plasticity in retrosplenial cortex. FENS Abstracts 3, A120.6.Google Scholar
Genin, A., Davis, S., Meziane, H., Doyere, V., Jeromin, A., Roder, J. et al. (2001) Regulated expression of the neuronal calcium sensor-1 gene during long-term potentiation in the dentate gyrus in vivo. Neuroscience 106, 571–577.CrossRefGoogle ScholarPubMed
Giles, P.J. and Kipling, D. (2003) Normality of oligonucleotide microarray data and implications for parametric statistical analyses. Bioinformatics 19, 2254–2262.CrossRefGoogle ScholarPubMed
Gonzalo-Ruiz, A. (1999) Alteraciones en los sistemas de neurotransmisión tras inyectar la proteína beta-amiloide ß(12-28) en el hipotálamo y en el tálamo anterior de la rata. Revista de Neurología 28, 931–941.CrossRefGoogle Scholar
Gonzalo-Ruiz, A., Sanz, J.M., Morte, L. and Lieberman, A.R. (1997) Glutamate and aspartate immunoreactivity in the reciprocal projections between the anterior thalamic nuclei and the retrosplenial granular cortex in the rat. Brain Research Bulletin 42, 309–321.Google ScholarPubMed
Harding, A., Halliday, G., Caine, D. and Kril, J. (2000) Degeneration of anterior thalamic nuclei differentiates alcoholics with amnesia. Brain 123, 141–154.CrossRefGoogle ScholarPubMed
Hertz, L. and Zielke, H.R. (2004) Astrocytic control of glutamatergic activity: astrocytes as stars of the show. Trends in Neuroscience 27, 735–743.CrossRefGoogle Scholar
Hirai, H., Pang, Z., Bao, D., Miyazaki, T., Li, L., Miura, E. et al. (2005) Cbln1 is essential for synaptic integrity and plasticity in the cerebellum. Nature Neuroscience 8, 1534–1541.CrossRefGoogle ScholarPubMed
Ho, L., Guo, Y., Spielman, L., Petrescu, O., Haroutunian, V., Purohit, D. et al. (2001) Altered expression of a-type but not b-type synapsin isoform in the brain of patients at high risk for Alzheimer's disease assessed by DNA microarray technique. Neuroscience Letters 298, 191–194.CrossRefGoogle Scholar
Holter, J.L., Humphries, A., Crunelli, V. and Carter, D.A. (2001) Optimisation of methods for selecting candidate genes from cDNA array screens: application to rat brain punches and pineal. Journal of Neuroscience Methods 112, 173–184.CrossRefGoogle ScholarPubMed
Hong, S.J., Li, H., Becker, K.G., Dawson, V.L. and Dawson, T.M. (2004) Identification and analysis of plasticity-induced late-response genes. Proceedings of the National Academy of Sciences of the United States of America 101, 2145–2150.CrossRefGoogle ScholarPubMed
Humphries, A., Klein, D., Baler, R. and Carter, D.A. (2002) cDNA array analysis of pineal gene expression reveals circadian rhythmicity of the dominant negative helix-loop-helix protein-encoding gene Id-1. Journal of Neuroendocrinology 14, 101–108.Google ScholarPubMed
Hwang, D.Y., Cho, J.S., Oh, J.H., Shim, S.B., Jee, S.W., Lee, S.H. et al. (2005) Differentially expressed genes in transgenic mice carrying human mutant presenilin-2 (N141I): Correlation of selenoprotein M with Alzheimer's disease. Neurochemical Research 30, 1009–1019.CrossRefGoogle ScholarPubMed
Hyder, F., Patel, A.B., Gjedde, A., Rothman, D.L., Behar, K.L. and Shulman, R.G. (2006) Neuronal-glial glucose oxidation and glutamatergic-GABAergic function. Journal of Cerebral Blood Flow and Metabolism 26, 865–877.CrossRefGoogle ScholarPubMed
Ichinohe, N. and Rockland, K.S. (2002) Parvalbumin positive dendrites co-localize with apical dendritic bundles in rat retrosplenial cortex. Neuroreport 13, 757–761.CrossRefGoogle ScholarPubMed
Insausti, R., Herrero, M.T. and Witter, M.P. (1997) Entorhinal cortex of the rat: Cytoarchitectonic subdivisions and the origin and distribution of cortical efferents. Hippocampus 7, 146–183.3.0.CO;2-L>CrossRefGoogle ScholarPubMed
Ishiki, M. and Klip, A. (2005) Minireview: Recent developments in the regulation of glucose transporter-4 traffic: New signals, locations, and partners. Endocrinology 146, 5071–5078.CrossRefGoogle ScholarPubMed
Jenkins, T.A., Vann, S.D., Amin, E. and Aggleton, J.P. (2004) Anterior thalamic lesions stop immediate early gene activation in selective laminae of the retrosplenial cortex: evidence of covert pathology in rats? European Journal of Neuroscience 19, 3291–3304.CrossRefGoogle ScholarPubMed
Johnson, K.A., Jones, K., Holman, B.L., Becker, J.A., Spiers, P.A., Satlin, A. et al. (1998) Preclinical prediction of Alzheimer's disease using SPECT. Neurology 50, 1563–1571.CrossRefGoogle ScholarPubMed
Jouvenceau, A., Hedou, G., Potier, B., Kollen, M., Dutar, P. and Mansuy, I.M. (2006) Partial inhibition of PP1 alters bidirectional synaptic plasticity in the hippocampus. European Journal of Neuroscience 24, 564–572.CrossRefGoogle ScholarPubMed
Kel, A.E., Gossling, E., Reuter, I., Cheremushkin, E., Kel-Margoulis, O.V. and Wingender, E. (2003) MATCH™: a tool for searching transcription factor binding sites in DNA sequences. Nucleic Acids Research 31, 3576–3579.CrossRefGoogle ScholarPubMed
Kogure, D., Matsuda, H., Ohnishi, T., Asada, T., Uno, M., Kunihiro, T. et al. (2000) Longitudinal evaluation of early Alzheimer's disease using brain perfusion SPECT. Journal of Nuclear Medicine 41, 1155–1162.Google ScholarPubMed
Krausz, Y., Freedman, N., Lester, H., Newman, J.P., Barkai, G., Bocher, M. et al. (2004) Regional cerebral blood flow in patients with mild hypothyroidism. Journal of Nuclear Medicine 45, 1712–1715.Google ScholarPubMed
Laurens, K.R., Kiehl, K.A., Ngan, E.T.C. and Liddle, P.F. (2005) Attention orienting dysfunction during salient novel stimulus processing in schizophrenia. Schizophrenia Research 75, 159–171.Google ScholarPubMed
Li, Q., Clark, S., Lewis, D.V. and Wilson, W.A. (2002) NMDA receptor antagonists disinhibit rat posterior cingulate and retrosplenial cortices: A potential mechanism of neurotoxicity. Journal of Neuroscience 22, 3070–3080.CrossRefGoogle ScholarPubMed
Lindecke, A., Korte, M., Zagrebelsky, M., Horejschi, V., Elvers, M., Widera, D. et al. (2006) Long-term depression activates transcription of immediate early transcription factor genes: involvement of serum response factor/Elk-1. European Journal of Neuroscience 24, 555–563.Google ScholarPubMed
Lorenzl, S., Albers, D.S., Relkin, N., Ngyuen, T., Hilgenberg, S.L., Chirichigno, J., Cudkowicz, M.E., Beal, M.F. (2003) Increased plasma levels of matrix metalloproteinase-9 in patients with Alzheimer's disease. Neurochemistry International 43, 191–196.CrossRefGoogle ScholarPubMed
Maguire, E. (2001) The retrosplenial contribution to human navigation: A review of lesion and neuroimaging findings. Scandinavian Journal of Psychology 42, 225–238.CrossRefGoogle ScholarPubMed
Marcus, D.L., Strafaci, J.A., Miller, D.C., Masia, S., Thomas, C.G., Rosman, J., Hussain, S., Freedman, M.L. (1998) Quantitative neuronal c-Fos and c-Jun expression in Alzheimer's disease. Neurobiology of Aging 19, 393–400.CrossRefGoogle ScholarPubMed
Marksteiner, J., Lechner, T., Kaufmann, W.A., Gurka, P., Humpel, C., Nowakowski, C., Maier, H., Jellinger, K.A. (2000) Distribution of chromogranin B-like immunoreactivity in the human hippocampus and its changes in Alzheimer's disease. Acta Neuropathologica 100, 205–212.CrossRefGoogle ScholarPubMed
Martinez-Bisbal, M.C., Arana, E., Marti-Bonmati, L., Molla, E. and Celda, B. (2004) Cognitive impairment: classification by 1H magnetic resonance spectroscopy. European Journal of Neurology 11, 187–193.CrossRefGoogle ScholarPubMed
Masliah, E., Terry, R. and Buzsaki, G. (1989) Thalamic nuclei in Alzheimer disease: evidence against the cholinergic hypothesis of plaque formation. Brain Research 493, 240–246.CrossRefGoogle ScholarPubMed
Matsuda, H., Kitayama, N., Ohnishi, T., Asada, T., Nakano, S., Sakamoto, S. et al. (2002) Longitudinal evaluation of both morphologic and functional changes in the same individuals with Alzheimer's disease. Journal of Nuclear Medicine 43, 304–311.Google ScholarPubMed
Matsuyama, S.C.A., Matsumoto, A., Hashimoto, H., Shintani, N. and Baba, A. (2003) Impaired long-term potentiation in vivo in the dentate gyrus of pituitary adenylate cyclase-activating polypeptide (PACAP) or PACAP type 1 receptor-mutant mice. Neuroreport 14, 2095–2098.Google ScholarPubMed
Meguro, K., Blaizot, X., Kondoh, Y., Le Mestric, C., Baron, J.C. and Chavoix, C. (1999) Neocortical and hippocampal glucose hypometabolism following neurotoxic lesions of the entorhinal and perirhinal cortices in the non-human primate as shown by PET: Implications for Alzheimer's disease. Brain 122, 1519–1531.CrossRefGoogle ScholarPubMed
Mi, R., Tang, X., Sutter, R., Xu, D., Worley, P. and O'Brien, R.J. (2002) Differing mechanisms for glutamate receptor aggregation on dendritic spines and shafts in cultured hippocampal neurons. Journal of Neuroscience 22, 7606–7616.CrossRefGoogle ScholarPubMed
Mingorance, A., Fontana, X., Soriano, E. and del Rio, J.A. (2005) Overexpression of myelin-associated glycoprotein after axotomy of the perforant pathway. Molecular and Cellular Neurosciences 29, 471–483.CrossRefGoogle ScholarPubMed
Minoshima, S., Giordani, B., Berent, S., Frey, K.A., Foster, N.L., Kuhl, D.E. (1997) Metabolic reduction in the posterior cingulate cortex in very early Alzheimer's disease. Annals of Neurology 42, 85–94.CrossRefGoogle ScholarPubMed
Mitelman, S.A., Shihabuddin, L., Brickman, A.M., Hazlett, E.A. and Buchsbaum, M.S. (2003) MRI assessment of gray and white matter distribution in Brodmann's areas of the cortex in patients with schizophrenia with good and poor outcomes. American Journal of Psychiatry 160, 2154–2168.Google ScholarPubMed
Mody, I. (2001) Distinguishing between GABA(A) receptors responsible for tonic and phasic conductances. Neurochemical Research 26, 907–913.CrossRefGoogle ScholarPubMed
Morishita, W., Connor, J.H., Xia, H., Quinlan, E.M., Shenolikar, S. and Malenka, R.C. (2001) Regulation of synaptic strength by protein phosphatase 1. Neuron 32, 1133–1148.CrossRefGoogle ScholarPubMed
Moroni, F. (1999) Tryptophan metabolism and brain function: focus on kynurenine and other indole metabolites. European Journal of Pharmacology 375, 87–100.CrossRefGoogle ScholarPubMed
Mulkey, R.M., Endo, S., Shenolikar, S. and Malenka, R.C. (1994) Involvement of a calcineurin/ inhibitor-1 phosphatase cascade in hippocampal long-term depression. Nature 369, 486–488.CrossRefGoogle ScholarPubMed
Murphy, D. (2002) Gene expression studies using microarrays: Principles, problems, and prospects. Advances in Physiology Education 26, 256–270.CrossRefGoogle Scholar
Nagy, V., Bozdagi, O., Matynia, A., Balcerzyk, M., Okulski, P., Dzwonek, J. et al. (2006) Matrix metalloproteinase-9 is required for hippocampal late-phase long-term potentiation and memory. Journal of Neuroscience 26, 1923–1934.CrossRefGoogle ScholarPubMed
Nestor, P.J., Fryer, T.D., Ikeda, M. and Hodges, J.R. (2003a) Retrosplenial cortex (BA 29/30) hypometabolism in mild cognitive impairment (prodromal Alzheimer's disease). European Journal of Neuroscience 18, 2663–2667.CrossRefGoogle ScholarPubMed
Nestor, P.J., Fryer, T.D., Smielewski, P. and Hodges, J.R. (2003b) Limbic hypometabolism in Alzheimer's disease and mild cognitive impairment. Annals of Neurology 54, 343–351.CrossRefGoogle ScholarPubMed
Newell, K.A., Zavitsanou, K. and Huang, X-F.C.A. (2005) Ionotropic glutamate receptor binding in the posterior cingulate cortex in schizophrenia patients. Neuroreport 16, 1363–1367.CrossRefGoogle ScholarPubMed
Nieto-Sampedro, M., Lewis, E.R., Cotman, C.W., Manthorpe, M., Skaper, S.D. and Barbin, G. et al. (1982) Brain injury causes a time-dependent increase in neuronotrophic activity at the lesion site. Science 217, 860–861.CrossRefGoogle ScholarPubMed
Norenberg, M.D. and Martinez-Hernandez, A. (1979) Fine structural localization of glutamine synthetase in astrocytes of rat brain. Brain Research 161, 303–310.CrossRefGoogle ScholarPubMed
O'Brien, R.J., Xu, D., Petralia, R.S., Steward, O., Huganir, R.L. and Worley, P. (1999) Synaptic clustering of AMPA receptors by the extracellular immediate-early gene product Narp. Neuron 23, 309–323.CrossRefGoogle ScholarPubMed
Ogita, K., Fujinami, Y., Kitano, M. and Yoneda, Y. (2003) Transcription factor activator protein-1 expressed by kainate treatment can bind to the non-coding region of mitochondrial genome in murine hippocampus. Journal of Neuroscience Research 73, 794–802.CrossRefGoogle Scholar
Ogita, K., Okuda, H., Kitano, M., Fujinami, Y., Ozaki, K. and Yoneda, Y. (2002) Localization of Activator Protein-1 complex with DNA binding activity in mitochondria of murine brain after in vivo treatment with kainate. Journal of Neuroscience 22, 2561–2570.CrossRefGoogle ScholarPubMed
Otto, C., Kovalchuk, Y., Wolfer, D.P., Gass, P., Martin, M., Zuschratter, W. et al. (2001) Impairment of mossy fiber long-term potentiation and associative learning in pituitary adenylate cyclase activating polypeptide type I receptor-deficient mice. Journal of Neuroscience 21, 5520–5527.CrossRefGoogle ScholarPubMed
Patel, A.B., de Graaf, R.A., Mason, G.F., Rothman, D.L., Shulman, R.G. and Behar, K.L. (2005) The contribution of GABA to glutamate/glutamine cycling and energy metabolism in the rat cortex in vivo. Proceedings of the National Academy of Sciences of the United States of America 102, 5588–5593.CrossRefGoogle ScholarPubMed
Pavlidis, P. (2003) Using ANOVA for gene selection from microarray studies of the nervous system. Methods 31, 282–289.CrossRefGoogle ScholarPubMed
Paxinos, G. and Watson, C. (1997) The Rat Brain in Stereotaxic Coordinates. Academic Press.Google Scholar
Pepicelli, O., Fedele, E., Berardi, M., Raiteri, M., Levi, G., Greco, A. et al. (2005) Cyclo-oxygenase-1 and -2 differently contribute to prostaglandin E2 synthesis and lipid peroxidation after in vivo activation of N-methyl-d-aspartate receptors in rat hippocampus. Journal of Neurochemistry 93, 1561–1567.CrossRefGoogle ScholarPubMed
Petrini, E.M., Marchionni, I., Zacchi, P., Sieghart, W. and Cherubini, E. (2004) Clustering of extrasynaptic GABAA receptors modulates tonic inhibition in cultured hippocampal neurons. Journal of Biological Chemistry 279, 45833–45843.CrossRefGoogle ScholarPubMed
Poirier, G. and Aggleton, J.P. (2006) The retrosplenial cortex and immediate-early gene reactivity following deafferentation in the rat. Experimental Psychology Society Abstract.Google Scholar
Poirier, G., Bloom, Z. and Aggleton, J.P. (2005) Temporal effect of anterior thalamic lesions on gene activation in retrosplenial cortex in the rat: Early appearance of “covert” pathology. European Brain and Behaviour Society Abstract.Google Scholar
Reed, L.J., Marsden, P., Lasserson, D., Sheldon, N., Lewis, P., Stanhope, N. et al. (1999) FDG-PET analysis and findings in amnesia resulting from hypoxia. Memory 7, 599–612.CrossRefGoogle ScholarPubMed
Reed, L.J., Lasserson, D., Marsden, P., Stanhope, N., Stevens, T., Bello, F. et al. (2003) FDG-PET findings in the Wernicke-Korsakoff syndrome. Cortex 39, 1027–1045.CrossRefGoogle ScholarPubMed
Roloff, E.L. and Platt, B. (1999) Biochemical dysfunction and memory loss: the case of Alzheimer's dementia. Cellular and Molecular Life Sciences 55, 601–616.CrossRefGoogle Scholar
Salmon, E., Collette, F., Degueldre, C., Lemaire, C. and Franck, G. (2000) Voxel-based analysis of confounding effects of age and dementia severity on cerebral metabolism in Alzheimer's disease. Human Brain Mapping 10, 39–48.3.0.CO;2-B>CrossRefGoogle ScholarPubMed
Savaskan, N.E., Brauer, A.U., Kuhbacher, M., Eyupoglu, I.Y., Kyriakopoulos, A., Ninnemann, O. et al. (2003) Selenium deficiency increases susceptibility to glutamate-induced excitotoxicity. FASEB Journal 17, 112–114.CrossRefGoogle ScholarPubMed
Schwieler, L., Erhardt, S., Erhardt, C. and Engberg, G. (2005) Prostaglandin-mediated control of rat brain kynurenic acid synthesis - opposite actions by COX-1 and COX-2 isoforms. Journal of Neural Transmission 112, 863–872.CrossRefGoogle ScholarPubMed
Selkoe, D.J. (2002) Alzheimer's disease is a synaptic failure. Science 298, 789–791.CrossRefGoogle ScholarPubMed
Shivers, B.D., Killisch, I., Sprengel, R., Sontheimer, H., Kohler, M., Schofield, P.R. et al. (1989) Two novel GABAA receptor subunits exist in distinct neuronal subpopulations. Neuron 3, 327–337.CrossRefGoogle ScholarPubMed
Small, D.H., Mok, S.S. and Bornstein, J.C. (2001) Alzheimer's disease and Abeta toxicity: from top to bottom. Nature Reviews Neuroscience 2, 595–598.CrossRefGoogle ScholarPubMed
Squire, L.R. and Zola, S.M. (1996) Ischemic brain damage and memory impairment: a commentary. Hippocampus 6, 546–552.3.0.CO;2-G>CrossRefGoogle ScholarPubMed
Subramanian, A., Tamayo, P., Mootha, V.K., Mukherjee, S., Ebert, B.L., Gillette, M.A. et al. (2005) Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles. Proceedings of the National Academy of Sciences of the United States of America 102, 15545–15550.CrossRefGoogle ScholarPubMed
Sugden, D. (2003) Comparison of circadian expression of tryptophan hydroxylase isoform mRNAs in the rat pineal gland using real-time PCR. Journal of Neurochemistry 86, 1308–1311.CrossRefGoogle ScholarPubMed
Sutherland, R.J. and Hoesing, J.M. (1993) Posterior cingulate cortex and spatial memory: A microlimnology analysis. In Vogt, B.A., Gabriel, M. (eds) Neurobiology of cingulate cortex and limbic thalamus: A comprehensive handbook. Birkhäuser. pp 461–477.CrossRefGoogle Scholar
Takano, T., Tian, G.-F., Peng, W., Lou, N., Libionka, W., Han, X. et al. (2006) Astrocyte-mediated control of cerebral blood flow. Nature Neuroscience 9, 260–267.CrossRefGoogle ScholarPubMed
Thomas, M. and Jankovic, J. (2004) Neurodegenerative disease and iron storage in the brain. Current Opinion in Neurology 17, 437–442.CrossRefGoogle ScholarPubMed
Valenstein, E., Bowers, D., Verfaellie, M., Heilman, K.M., Day, A. and Watson, R.T. (1987) Retrosplenial amnesia. Brain 110, 1631–1646.CrossRefGoogle ScholarPubMed
Valla, J., Berndt, J.D. and Gonzalez-Lima, F. (2001) Energy hypometabolism in posterior cingulate cortex of Alzheimer's patients: superficial laminar cytochrome oxidase associated with disease duration. Journal of Neuroscience 21, 4923–4930.CrossRefGoogle ScholarPubMed
van der Werf, Y.D., Scheltens, P., Lindeboom, J., Witter, M.P., Uylings, H.B.M. and Jolles, J. (2003) Deficits of memory, executive functioning and attention following infarction in the thalamus; a study of 22 cases with localised lesions. Neuropsychologia 41, 1330–1344.CrossRefGoogle ScholarPubMed
van Groen, T. and Wyss, J.M. (2003) Connections of the retrosplenial granular b cortex in the rat. Journal of Comparative Neurology 463, 249–263.CrossRefGoogle ScholarPubMed
van Groen, T., Vogt, B.A. and Wyss, J.M. (1993) Interconnections between the thalamus and retrosplenial cortex in the rodent brain. In Vogt, B.A., Gabriel, M. (eds) Neurobiology of cingulate cortex and limbic thalamus: A comprehensive handbook. Birkhäuser. pp. 123–150.CrossRefGoogle Scholar
Vaynman, S., Ying, Z., Wu, A. and Gomez-Pinilla, F. (2006) Coupling energy metabolism with a mechanism to support brain-derived neurotrophic factor-mediated synaptic plasticity. Neuroscience 139, 1221–1234.CrossRefGoogle ScholarPubMed
Vogt, B.A. and Peters, A. (1981) Form and distribution of neurons in rat cingulate cortex: Areas 32, 24, and 29. Journal of Comparative Neurology 195, 603–625.CrossRefGoogle Scholar
Vogt, B.A., Rosene, D.L. and Peters, A. (1981) Synaptic termination of thalamic and callosal afferents in cingulate cortex of the rat. Journal of Comparative Neurology 201, 265–283.CrossRefGoogle ScholarPubMed
Wenstrup, D., Ehman, W.D. and Markesbery, W.R. (1990) Trace element imbalances in isolated subcellular fractions of Alzheimer's disease brains. Brain Research 533, 125–131.CrossRefGoogle ScholarPubMed
White, A.-M. and Platt, B. (2001) Ionic mechanisms of GABA-induced long-term potentiation in the rat superior colliculus. Experimental Brain Research 140, 486–494.CrossRefGoogle ScholarPubMed
Wibrand, K., Messaoudi, E., Havik, B., Steenslid, V., Lovlie, R., Steen, V.M. et al. (2006) Identification of genes co-upregulated with Arc during BDNF-induced long-term potentiation in adult rat dentate gyrus in vivo. European Journal of Neuroscience 23, 1501–1511.CrossRefGoogle ScholarPubMed
Williams, J.M., Thompson, V.L., Mason-Parker, S.E., Abraham, W.C. and Tate, W.P. (1998) Synaptic activity-dependent modulation of mitochondrial gene expression in the rat hippocampus. Brain Research. Molecular Brain Research 60, 50–56.CrossRefGoogle ScholarPubMed
Wisden, W. and Morris, B.J. (1994) In situ hybridization with synthetic oligonucleotide probes. In Wisden, W. and Morris, B.J. (eds) In situ hybridization protocols for the brain. Academic Press, pp 9–34.Google Scholar
Yao, P.J., Zhu, M., Pyun, E.I., Brooks, A.I., Therianos, S., Meyers, V.E. et al. (2003) Defects in expression of genes related to synaptic vesicle trafficking in frontal cortex of Alzheimer's disease. Neurobiology of Disease 12, 97–109.CrossRefGoogle ScholarPubMed
Yunfeng, L., Yongsheng, C., Lifeng, Z., Qiping, F., Zhuo, L., Yongwei, Z. et al. (2005) High glucose upregulates pantothenate kinase 4 (PanK4) and thus affects M2-type pyruvate kinase (Pkm2). Molecular and Cellular Biochemistry 277, 117–125.Google Scholar