Lack of cyclin D2 impairing adult brain neurogenesis alters hippocampal-dependent behavioral tasks without reducing learning ability

Behavioural Brain Research

Volumn 227, Issue 1, 2012, Pages 159-166

  Jedynak, Paulina ^a   Jaholkowski, Piotr ^a   Wozniak, Grazyna ^a   Sandi, Carmen ^b   Kaczmarek, Leszek ^a   Filipkowski, Robert K ^c  

^a NENCKI INSTITUTE OF EXPERIMENTAL BIOLOGY   (Poland)

^b EPFL   (Switzerland)

^c UNIVERSITY OF FINANCE AND MANAGEMENT   (Poland)

Author keywords

Adult neurogenesis; Hippocampal formation; Hippocampal tasks; Knockout mice; Rodent specific behaviors

Indexed keywords

CYCLIN D2; SUCROSE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR; BRAIN DEVELOPMENT; BRAIN SIZE; CONTROLLED STUDY; CYCLIN D2 GENE; DEVELOPMENTAL DISORDER; EXPLORATORY BEHAVIOR; FOOD PREFERENCE; GENE; GENE SILENCING; HIPPOCAMPUS; LEARNING; LEARNING DISORDER; LOCOMOTION; MEMORY DISORDER; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SPECIES DIFFERENCE;

ANALYSIS OF VARIANCE; ANIMALS; BRAIN; BROMODEOXYURIDINE; CELL COUNT; CONDITIONING (PSYCHOLOGY); CUES; CYCLIN D2; DRINKING; EXPLORATORY BEHAVIOR; FEAR; FOOD PREFERENCES; GROOMING; HIPPOCAMPUS; LEARNING DISORDERS; MAZE LEARNING; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MOTOR ACTIVITY; NESTING BEHAVIOR; NEUROGENESIS; ORGAN SIZE; REACTION TIME;

EID: 82255161805     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2011.11.007     Document Type: Article

References (48)

1. Jaholkowski P., Kiryk A., Jedynak P., Ben Abdallah N.M., Knapska E., Kowalczyk A., et al. New hippocampal neurons are not obligatory for memory formation; cyclin D2 knockout mice with no adult brain neurogenesis show learning. Learning & Memory 2009, 16:439-451.
2. Kowalczyk A., Filipkowski R.K., Rylski M., Wilczynski G.M., Konopacki F.A., Jaworski J., et al. The critical role of cyclin D2 in adult neurogenesis. Journal of Cell Biology 2004, 167:209-213.
3. Antonawich F.J., Melton C.S., Wu P., Davis J.N. Nesting and shredding behavior as an indicator of hippocampal ischemic damage. Brain Research 1997, 764:249-252.
4. Deacon R.M., Croucher A., Rawlins J.N. Hippocampal cytotoxic lesion effects on species-typical behaviours in mice. Behavioural Brain Research 2002, 132:203-213.
5. Deacon R.M., Raley J.M., Perry V.H., Rawlins J.N. Burrowing into prion disease. Neuroreport 2001, 12:2053-2057.
6. Deacon R.M., Rawlins J.N. Hippocampal lesions, species-typical behaviours and anxiety in mice. Behavioural Brain Research 2005, 156:241-249.
7. Guenther K., Deacon R.M., Perry V.H., Rawlins J.N. Early behavioural changes in scrapie-affected mice and the influence of dapsone. The European Journal of Neuroscience 2001, 14:401-409.
8. Good M., Honey R.C. Dissociable effects of selective lesions to hippocampal subsystems on exploratory behavior, contextual learning, and spatial learning. Behavioral Neuroscience 1997, 111:487-493.
9. Sicinski P., Donaher J.L., Geng Y., Parker S.B., Gardner H., Park M.Y., et al. Cyclin D2 is an FSH-responsive gene involved in gonadal cell proliferation and oncogenesis. Nature 1996, 384:470-474.
10. Deacon R.M. Burrowing in rodents: a sensitive method for detecting behavioral dysfunction. Nature Protocols 2006, 1:118-121.
11. Knapska E., Maren S. Reciprocal patterns of c-Fos expression in the medial prefrontal cortex and amygdala after extinction and renewal of conditioned fear. Learning & Memory 2009, 16:486-493.
12. Saxe M.D., Battaglia F., Wang J.W., Malleret G., David D.J., Monckton J.E., et al. Ablation of hippocampal neurogenesis impairs contextual fear conditioning and synaptic plasticity in the dentate gyrus. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:17501-17506.
13. Deacon R.M. Digging and marble burying in mice: simple methods for in vivo identification of biological impacts. Nature Protocols 2006, 1:122-124.
14. Kalueff A.V., Keisala T., Minasyan A., Kuuslahti M., Miettinen S., Tuohimaa P. Behavioural anomalies in mice evoked by Tokyo disruption of the vitamin D receptor gene. Neuroscience Research 2006, 54:254-260.
15. Banbury Mutant mice and neuroscience: recommendations concerning genetic background. Banbury Conference on genetic background in mice. Neuron 1997, 19:755-759.
16. Shors T.J., Townsend D.A., Zhao M., Kozorovitskiy Y., Gould E. Neurogenesis may relate to some but not all types of hippocampal-dependent learning. Hippocampus 2002, 12:578-584.
17. Zhang C.L., Zou Y., He W., Gage F.H., Evans R.M. A role for adult TLX-positive neural stem cells in learning and behaviour. Nature 2008, 451:1004-1007.
18. Deacon R.M., Bannerman D.M., Kirby B.P., Croucher A., Rawlins J.N. Effects of cytotoxic hippocampal lesions in mice on a cognitive test battery. Behavioural Brain Research 2002, 133:57-68.
19. Deacon R.M., Penny C., Rawlins J.N. Effects of medial prefrontal cortex cytotoxic lesions in mice. Behavioural Brain Research 2003, 139:139-155.
20. Lacroix L., Broersen L.M., Weiner I., Feldon J. The effects of excitotoxic lesion of the medial prefrontal cortex on latent inhibition, prepulse inhibition, food hoarding, elevated plus maze, active avoidance and locomotor activity in the rat. Neuroscience 1998, 84:431-442.
21. Yee B.K. Cytotoxic lesion of the medial prefrontal cortex abolishes the partial reinforcement extinction effect, attenuates prepulse inhibition of the acoustic startle reflex and induces transient hyperlocomotion, while sparing spontaneous object recognition memory in the rat. Neuroscience 2000, 95:675-689.
22. Glickman S.E., Higgins T.J., Isaacson R.L. Some effects of hippocampal lesions on the behavior of Mongolian gerbils. Physiology & Behavior 1970, 5:931-938.
23. Kim C. Nest building, general activity, and salt preference of rats following hippocampal ablation. Journal of Comparative and Physiological Psychology 1960, 53:11-16.
24. Kimble D.P., Rogers L., Hendrickson C.W. Hippocampal lesions disrupt maternal, not sexual, behavior in the albino rat. Journal of Comparative and Physiological Psychology 1967, 63:401-407.
25. Murphy H.M., Brown T.S. Effects of hippocampal lesions on simple and preferential consummatory behavior in the rat. Journal of Comparative and Physiological Psychology 1970, 72:404-415.
26. Bremner J.D., Narayan M., Anderson E.R., Staib L.H., Miller H.L., Charney D.S. Hippocampal volume reduction in major depression. The American Journal of Psychiatry 2000, 157:115-118.
27. Brown G.G., Lee J.S., Strigo I.A., Caligiuri M.P., Meloy M.J., Lohr J. Voxel-based morphometry of patients with schizophrenia or bipolar I disorder: a matched control study. Psychiatry Research 2011, 194:149-156.
28. Zorner B., Wolfer D.P., Brandis D., Kretz O., Zacher C., Madani R., et al. Forebrain-specific trkB-receptor knockout mice: behaviorally more hyperactive than depressive. Biological Psychiatry 2003, 54:972-982.
29. Kimble D.P. The effects of bilateral hippocampal lesions in rats. Journal of Comparative and Physiological Psychology 1963, 56:273-283.
30. Mickley G.A., Ferguson J.L., Nemeth T.J., Mulvihill M.A., Alderks C.E. Spontaneous perseverative turning in rats with radiation-induced hippocampal damage. Behavioral Neuroscience 1989, 103:722-730.
31. Onksen J.L., Brown E.J., Blendy J.A. Selective Deletion of a cell cycle checkpoint kinase (ATR) reduces neurogenesis and alters responses in rodent models of behavioral affect. Neuropsychopharmacology 2011, 36:960-969.
32. Dagyte G., Crescente I., Postema F., Seguin L., Gabriel C., Mocaer E., et al. Agomelatine reverses the decrease in hippocampal cell survival induced by chronic mild stress. Behavioural Brain Research 2011, 218:121-128.
33. Kitamura T., Saitoh Y., Takashima N., Murayama A., Niibori Y., Ageta H., et al. Adult neurogenesis modulates the hippocampus-dependent period of associative fear memory. Cell 2009, 139:814-827.
34. Rola R., Raber J., Rizk A., Otsuka S., VandenBerg S.R., Morhardt D.R., et al. Radiation-induced impairment of hippocampal neurogenesis is associated with cognitive deficits in young mice. Experimental Neurology 2004, 188:316-330.
35. Saxe M.D., Malleret G., Vronskaya S., Mendez I., Garcia A.D., Sofroniew M.V., et al. Paradoxical influence of hippocampal neurogenesis on working memory. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:4642-4646.
36. Shors T.J., Miesegaes G., Beylin A., Zhao M., Rydel T., Gould E. Neurogenesis in the adult is involved in the formation of trace memories. Nature 2001, 410:372-376.
37. Faivre E., Gault V.A., Thorens B., Holscher C. Glucose-dependent insulinotropic polypeptide receptor knockout mice are impaired in learning, synaptic plasticity, and neurogenesis. Journal of Neurophysiology 2011.
38. Shen L., Nam H.S., Song P., Moore H., Anderson S.A. FoxG1 haploinsufficiency results in impaired neurogenesis in the postnatal hippocampus and contextual memory deficits. Hippocampus 2006, 16:875-890.
39. Santarelli L., Saxe M., Gross C., Surget A., Battaglia F., Dulawa S., et al. Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 2003, 301:805-809.
40. van Praag H., Christie B.R., Sejnowski T.J., Gage F.H. Running enhances neurogenesis, learning, and long-term potentiation in mice. Proceedings of the National Academy of Sciences of the United States of America 1999, 96:13427-13431.
41. van Praag H., Kempermann G., Gage F.H. Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nature Neuroscience 1999, 2:266-270.
42. Fuss J., Ben Abdallah N.M., Hensley F.W., Weber K.J., Hellweg R., Gass P. Deletion of running-induced hippocampal neurogenesis by irradiation prevents development of an anxious phenotype in mice. PloS One 2010, 5:e12769.
43. Meshi D., Drew M.R., Saxe M., Ansorge M.S., David D., Santarelli L., et al. Hippocampal neurogenesis is not required for behavioral effects of environmental enrichment. Nature Neuroscience 2006, 9:729-731.
44. Revest J.M., Dupret D., Koehl M., Funk-Reiter C., Grosjean N., Piazza P.V., et al. Adult hippocampal neurogenesis is involved in anxiety-related behaviors. Molecular Psychiatry 2009, 14:959-967.
45. Ageta H., Murayama A., Migishima R., Kida S., Tsuchida K., Yokoyama M., et al. Activin in the brain modulates anxiety-related behavior and adult neurogenesis. PloS One 2008, 3:e1869.
46. Bergami M., Rimondini R., Santi S., Blum R., Gotz M., Canossa M. Deletion of TrkB in adult progenitors alters newborn neuron integration into hippocampal circuits and increases anxiety-like behavior. Proceedings of the National Academy of Sciences of the United States of America 2008, 105:15570-15575.
47. Fuss J., Ben Abdallah N.M., Vogt M.A., Touma C., Pacifici P.G., Palme R., et al. Voluntary exercise induces anxiety-like behavior in adult C57BL/6J mice correlating with hippocampal neurogenesis. Hippocampus 2010, 20:364-376.
48. Jimenez-Gomez C., Osentoski A., Woods J.H. Pharmacological evaluation of the adequacy of marble burying as an animal model of compulsion and/or anxiety. Behavioural Pharmacology 2011, 22:711-713.