Environmental novelty is associated with a selective increase in Fos expression in the output elements of the hippocampal formation and the perirhinal cortex

Learning and Memory

Volumn 15, Issue 12, 2008, Pages 899-908

  VanElzakker, Michael ^a   Fevurly, Rebecca D ^a   Breindel, Tressa ^a   Spencer, Robert L ^a  

^a UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN FOS;

ANIMAL EXPERIMENT; ANTERIOR HYPOTHALAMUS; ANXIETY; ARTICLE; BRAIN CORTEX; BRAIN REGION; CONTROLLED STUDY; DENTATE GYRUS; ENTORHINAL CORTEX; ENVIRONMENTAL FACTOR; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MALE; MOBILIZATION; MOTOR ACTIVITY; MOTOR CORTEX; NERVE CELL; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; RAT; SIGNAL TRANSDUCTION; SOMATOSENSORY CORTEX; SYNAPTIC TRANSMISSION; UPREGULATION;

ANALYSIS OF VARIANCE; ANIMALS; CELL COUNT; ENVIRONMENT; EXPLORATORY BEHAVIOR; GENE EXPRESSION REGULATION; HIPPOCAMPUS; LINEAR MODELS; MALE; ONCOGENE PROTEINS V-FOS; PREFRONTAL CORTEX; RATS; RATS, SPRAGUE-DAWLEY; SPATIAL BEHAVIOR;

EID: 57349170839     PISSN: 10720502     EISSN: 15495485     Source Type: Journal    
DOI: 10.1101/lm.1196508     Document Type: Article

References (52)

1. Andersen, P., Bliss, T.V.P., and Skrede, K.K. 1971. Lamellar organization of hippocampal excitatory pathways. Exp. Brain Res. 13: 222-238.
2. Brecht, M., Schneider, M., Sakmann, B., and Margrie, T.W. 2004. Whisker movements evoked by stimulation of single pyramidal cells in rat motor cortex. Nature 427: 704-710.
3. Brown, M.W. and Aggleton, J.P. 2001. Recognition memory: What are the roles of the perirhinal cortex and hippocampus? Nat. Rev. Neurosci. 2: 51-61.
4. Bussey, T.J., Duck, J., Muir, J.L., and Aggleton, J.P. 2000. Distinct patterns of behavioural impairments resulting from fornix transection or neurotoxic lesions of the perirhinal and postrhinal cortices in the rat. Behav. Brain Res. 111: 187-202.
5. Choi, Y.S., Lee, M.Y., Sung, K.W., Jeong, S.W., Choi, J.S., Park, H.J., Kim, O.N., Lee, S.B., and Kim, S.Y. 2003. Regional differences in enhanced neurogenesis in the dentate gyrus of adult rats after transient forebrain ischemia. Mol. Cells 16: 232-238.
6. Chowdhury, G.M., Fujioka, T., and Nakamura, S. 2000. Induction and adaptation of Fos expression in the rat brain by two types of acute restraint stress. Brain Res. Bull. 52: 171-182.
7. Fevurly, R.D. and Spencer, R.L. 2004. Fos expression is selectively and differentially regulated by endogenous glucocorticoids in the paraventricular nucleus of the hypothalamus and the dentate gyrus. J. Neuroendocrinol. 16: 970-979.
8. Furtak, S.C., Wei, S.M., Agster, K.L., and Burwell, R.D. 2007. Functional neuroanatomy of the parahippocampal region in the rat: The perirhinal and postrhinal cortices. Hippocampus 17: 709-722.
9. Fyhn, M., Molden, S., Hollup, S., Moser, M.B., and Moser, E. 2002. Hippocampal neurons responding to first-time dislocation of a target object. Neuron 35: 555-566.
10. Gilbert, P.E., Kesner, R.P., and Lee, I. 2001. Dissociating hippocampal subregions: Double dissociation between dentate gyrus and CA1. Hippocampus 11: 626-636.
11. Guzowski, J.F., Miyashita, T., Chawla, M.K., Sanderson, J., Maes, L.I., Houston, F.P., Lipa, P., McNaughton, B.L., Worley, P.F., and Barnes, C.A. 2006. Recent behavioral history modifies coupling between cell activity and Arc gene transcription in hippocampal CA1 neurons. Proc. Natl. Acad. Sci. 103: 1077-1082.
12. Hartmann, D., Sievers, J., Pehlemann, F.W., and Berry, M. 1992. Destruction of meningeal cells over the medial cerebral hemisphere of newborn hamsters prevents the formation of the infrapyramidal blade of the dentate gyrus. J. Comp. Neurol. 320: 33-61.
13. Hasselmo, M.E. and Schnell, E. 1994. Laminar selectivity of the cholinergic suppression of synaptic transmission in rat hippocampal region CA1: Computational modeling and brain slice physiology. J. Neurosci. 14: 3898-3914.
14. Herdegen, T. and Leah, J.D. 1998. Inducible and constitutive transcription factors in the mammalian nervous system: Control of gene expression by Jun, Fos and Krox, and CREB/ATF proteins. Brain Res. Brain Res. Rev. 28: 370-490.
15. Hess, U.S., Lynch, G., and Gall, C.M. 1995a. Regional patterns of c-fos mRNA expression in rat hippocampus following exploration of a novel environment versus performance of a well-learned discrimination. J. Neurosci. 15: 7796-7809.
16. Hess, U.S., Lynch, G., and Gall, C.M. 1995b. Changes in c-fos mRNA expression in rat brain during odor discrimination learning: Differential involvement of hippocampal subfields CA1 and CA3. J. Neurosci. 15: 4786-4795.
17. Honey, R.C., Watt, A., and Good, M. 1998. Hippocampal lesions disrupt an associative mismatch process. J. Neurosci. 18: 2226-2230.
18. Johnson, J.D., Muftuler, L.T., and Rugg, M.D. 2008. Multiple repetitions reveal functionally and anatomically distinct patterns of hippocampal activity during continuous recognition memory. Hippocampus 18: 975-980.
19. Kim, S.Y., Min, D.S., Choi, J.S., Choi, Y.S., Park, H.J., Sung, K.W., Kim, J., and Lee, M.Y. 2004. Differential expression of phospholipase D isozymes in the hippocampus following kainic acid-induced seizures. J. Neuropathol. Exp. Neurol. 63: 812-820.
20. Knight, R. 1996. Contribution of human hippocampal region to novelty detection. Nature 383: 256-259.
21. Kumaran, D. and Maguire, E.A. 2007. Which computational mechanisms operate in the hippocampus during novelty detection? Hippocampus 17: 735-748.
22. Labiner, D.M., Butler, L.S., Cao, Z., Hosford, D.A., Shin, C., and McNamara, J.O. 1993. Induction of c-fos mRNA by kindled seizures: Complex relationship with neuronal burst firing. J. Neurosci. 13: 744-751.
23. Lee, I., Hunsaker, M.R., and Kesner, R.P. 2005a. The role of hippocampal subregions in detecting spatial novelty. Behav. Neurosci. 119: 145-153.
24. Lee, I., Jerman, T.S., and Kesner, R.P. 2005b. Disruption of delayed memory for a sequence of spatial locations following CA1- or CA3-lesions of the dorsal hippocampus. Neurobiol. Learn. Mem. 84: 138-147.
25. Margulies, D.M. 1985. Selective attention and the brain: A hypothesis concerning the hippocampal-ventral striatal axis, the mediation of selective attention, and the pathogenesis of attentional disorders. Med. Hypotheses 18: 221-264.
26. Meeter, M., Murre, J.M., and Talamini, L.M. 2004. Mode shifting between storage and recall based on novelty detection in oscillating hippocampal circuits. Hippocampus 14: 722-741.
27. Melzer, P. and Steiner, H. 1997. Stimulus-dependent expression of immediate-early genes in rat somatosensory cortex. J. Comp. Neurol. 380: 145-153.
28. Mizumori, S.J., Ragozzino, K.E., Cooper, B.G., and Leutgeb, S. 1999. Hippocampal representational organization and spatial context. Hippocampus 9: 444-451.
29. Montag-Sallaz, M., Welzl, H., Kuhl, D., Montag, D., and Schachner, M. 1999. Novelty-induced increased expression of immediate-early genes c-fos and arg 3.1 in the mouse brain. J. Neurobiol. 38: 234-246.
30. Moser, E.I. and Paulsen, O. 2001. New excitement in cognitive space: Between place cells and spatial memory. Curr. Opin. Neurobiol. 11: 745-751.
31. Mumby, D.G. and Pinel, J.P. 1994. Rhinal cortex lesions and object recognition in rats. Behav. Neurosci. 108: 11-18.
32. Mumby, D.G., Gaskin, S., Glenn, M.J., Schramek, T.E., and Lehmann, H. 2002. Hippocampal damage and exploratory preferences in rats: Memory for objects, places, and contexts. Learn. Mem. 9: 49-57.
33. Mumby, D.G., Piterkin, P., Lecluse, V., and Lehmann, H. 2007. Perirhinal cortex damage and anterograde object-recognition in rats after long retention intervals. Behav. Brain Res. 185: 82-87.
34. Nitz, D. and McNaughton, B. 2004. Differential modulation of CA1 and dentate gyrus interneurons during exploration of novel environments. J. Neurophysiol. 91: 863-872.
35. Norman, K.A. and O'Reilly, R.C. 2003. Modeling hippocampal and neocortical contributions to recognition memory: A complementary-learning- systems approach. Psychol. Rev. 110: 611-646.
36. Otto, T. and Eichenbaum, H. 1992. Neuronal activity in the hippocampus during delayed non-match to sample performance in rats: Evidence for hippocampal processing in recognition memory. Hippocampus 2: 323-334.
37. Pace, T.W., Gaylord, R., Topczewski, F., Girotti, M., Rubin, B., and Spencer, R.L. 2005. Immediate-early gene induction in hippocampus and cortex as a result of novel experience is not directly related to the stressfulness of that experience. Eur. J. Neurosci. 22: 1679-1690.
38. Paxinos, G. and Watson, C. 1998. The rat brain in stereotaxic coordinates, 4th ed. Academic, San Diego, CA.
39. Remondes, M. and Schuman, E.M. 2004. Role for a cortical input to hippocampal area CA1 in the consolidation of a long-term memory. Nature 431: 699-703.
40. Rudy, J.W. and Sutherland, R.J. 1995. Configural association theory and the hippocampal formation: An appraisal and reconfiguration. Hippocampus 5: 375-389.
41. Save, E., Poucet, B., Foreman, N., and Buhot, M.C. 1992. Object exploration and reactions to spatial and nonspatial changes in hooded rats following damage to parietal cortex or hippocampal formation. Behav. Neurosci. 106: 447-456.
42. Scharfman, H.E., Sollas, A.L., Smith, K.L., Jackson, M.B., and Goodman, J.H. 2002. Structural and functional asymmetry in the normal and epileptic rat dentate gyrus. J. Comp. Neurol. 454: 424-439.
43. Sheng, M. and Greenberg, M.E. 1990. The regulation and function of c-fos and other immediate early genes in the nervous system. Neuron 4: 477-485.
44. Stern, C.E., Corkin, S., González, R.G., Guimaraes, A.R., Baker, J.R., Jennings, P.J., Carr, C.A., Sugiura, R.M., Vedantham, V., and Rosen, B.R. 1996. The hippocampal formation participates in novel picture encoding: Evidence from functional magnetic resonance imaging. Proc. Natl. Acad. Sci. 93: 8660-8665.
45. Steward, O. and Scoville, S.A. 1976. Cells of origin of entorhinal cortical afferents to the hippocampus and fascia dentata of the rat. J. Comp. Neurol. 169: 347-370.
46. Strekalova, T., Zörner, B., Zacher, C., Sadovska, G., Herdegen, T., and Gass, P. 2003. Memory retrieval after contextual fear conditioning induces c-Fos and JunB expression in CA1 hippocampus. Genes Brain Behav. 2: 3-10.
47. Tamamaki, N. 1997. Organization of the entorhinal projection to the rat dentate gyrus revealed by Dil anterograde labeling. Exp. Brain Res. 116: 250-258.
48. Vann, S.D., Brown, M.W., Erichsen, J.T., and Aggleton, J.P. 2000. Fos imaging reveals differential patterns of hippocampal and parahippocampal subfield activation in rats in response to different spatial memory tests. J. Neurosci. 20: 2711-2718.
49. Vinogradova, O.S. 2001. Hippocampus as comparator: Role of the two input and two output systems of the hippocampus in selection and registration of information. Hippocampus 11: 578-598.
50. Wan, H., Aggleton, J.P., and Brown, M.W. 1999. Different contributions of the hippocampus and perirhinal cortex to recognition memory. J. Neurosci. 19: 1142-1148.
51. Witter, M. and Amaral, D. 2004. Hippocampal formation. In The rat nervous system, 3rd ed. (ed. G. Paxinos), pp. 635-704. Elsevier, Amsterdam.
52. Zhu, X.O., McCabe, B.J., Aggleton, J.P., and Brown, M.W. 1997. Differential activation of the rat hippocampus and perirhinal cortex by novel visual stimuli and a novel environment. Neurosci. Lett. 229: 141-143.