Ionizing Radiation Impairs the Formation of Trace Fear Memories and Reduces Hippocampal Neurogenesis

Behavioral Neuroscience

Volumn 123, Issue 5, 2009, Pages 1036-1045

  Achanta, Pragathi ^a,b   Fuss, Martin ^c   Martinez Jr , Joe L ^a  

^a UNIVERSITY OF TEXAS AT SAN ANTONIO   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

^c OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

fear conditioning; hippocampus; ionizing radiation; learning and memory; neurogenesis

Indexed keywords

BROXURIDINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASSOCIATIVE MEMORY; BRAIN FUNCTION; BRAIN RADIATION; CONDITIONED REFLEX; CONTROLLED STUDY; FEAR; FREEZING; GRANULE CELL; GROUPS BY AGE; HIPPOCAMPUS; IONIZING RADIATION; MALE; MEMORY; MEMORY DISORDER; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PERINATAL PERIOD; RADIATION DOSE; RAT; STIMULUS RESPONSE; TASK PERFORMANCE;

AGE FACTORS; ANALYSIS OF VARIANCE; ANIMALS; BROMODEOXYURIDINE; CELL COUNT; CONDITIONING, CLASSICAL; DOSE-RESPONSE RELATIONSHIP, RADIATION; FEAR; FREEZING REACTION, CATALEPTIC; HIPPOCAMPUS; MALE; MEMORY; NEUROGENESIS; NEURONS; RADIATION, IONIZING; RATS; RATS, SPRAGUE-DAWLEY;

EID: 70350118712     PISSN: 07357044     EISSN: None     Source Type: Journal    
DOI: 10.1037/a0016870     Document Type: Article

References (47)

1. Abayomi O.K. Pathogenesis of irradiation-induced cognitive dysfunction. Acta Oncologica 35 (1996) 659-663
2. Altman J., and Das G.D. Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. Journal of Comparative Neurology 124 (1965) 319-335
3. Andratschke N.H., Nieder C., Price R.E., Rivera B., Tucker S.L., and Ang K.K. Modulation of rodent spinal cord radiation tolerance by administration of platelet-derived growth factor. International Journal of Radiation Oncology, Biology, Physics 60 (2004) 1257-1263
4. Bayer S.A. Development of the hippocampal region in the rat. I. Neurogenesis examined with 3H-thymidine autoradiography. Journal of Comparative Neurology 190 (1980) 87-114
5. Bayer S.A. Changes in the total number of dentate granule cells in juvenile and adult rats: A correlated volumetric and 3H-thymidine autoradiographic study. Experimental Brain Research 46 (1982) 315-323
6. Cameron H.A., and McKay R.D. Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. Journal of Comparative Neurology 435 (2001) 406-417
7. Coderre J.A., Morris G.M., Micca P.L., Hopewell J.W., Verhagen I., Kleiboer B.J., et al. Late effects of radiation on the central nervous system: Role of vascular endothelial damage and glial stem cell survival. Radiation Research 166 (2006) 495-503
8. Crossen J.R., Garwood D., Glatstein E., and Neuwelt E.A. Neurobehavioral sequelae of cranial irradiation in adults: A review of radiation-induced encephalopathy. Journal of Clinical Oncology 12 (1994) 627-642
9. Esclassan F., Coutureau E., Di Scala G., and Marchand A.R. Differential contribution of dorsal and ventral hippocampus to trace and delay fear conditioning. Hippocampus 19 (2009) 33-44
10. Fan Y., Liu Z., Weinstein P.R., Fike J.R., and Liu J. Environmental enrichment enhances neurogenesis and improves functional outcome after cranial irradiation. European Journal of Neuroscience 25 (2007) 38-46
11. Fukuda H., Fukuda A., Zhu C., Korhonen L., Swanpalmer J., Hertzman S., et al. Irradiation-induced progenitor cell death in the developing brain is resistant to erythropoietin treatment and caspase inhibition. Cell Death and Differentiation 11 (2004) 1166-1178
12. Fuss M., Poljanc K., and Hug E.B. Full Scale IQ (FSIQ) changes in children treated with whole brain and partial brain irradiation. A review and analysis. Strahlentherapie Und Onkologie 176 (2000) 573-581
13. Gerlai R. Behavioral tests of hippocampal function: Simple paradigms complex problems. Behavioural Brain Research 125 (2001) 269-277
14. Gewirtz J.C., McNish K.A., and Davis M. Is the hippocampus necessary for contextual fear conditioning?. Behavioural Brain Research 110 (2000) 83-95
15. Hastings N.B., and Gould E. Rapid extension of axons into the CA3 region by adult-generated granule cells. Journal of Comparative Neurology 413 (1999) 146-154
16. Hodges H., Katzung N., Sowinski P., Hopewell J.W., Wilkinson J.H., Bywaters T., et al. Late behavioural and neuropathological effects of local brain irradiation in the rat. Behavioural Brain Research 91 (1998) 99-114
17. Huerta P.T., Sun L.D., Wilson M.A., and Tonegawa S. Formation of temporal memory requires NMDA receptors within CA1 pyramidal neurons. Neuron 25 (2000) 473-480
18. Kee N., Sivalingam S., Boonstra R., and Wojtowicz J.M. The utility of Ki-67 and BrdU as proliferative markers of adult neurogenesis. Journal of Neuroscience Methods 115 (2002) 97-105
19. Kesner R.P., Lee I., and Gilbert P. A behavioral assessment of hippocampal function based on a subregional analysis. Reviews in the Neurosciences 15 (2004) 333-351
20. Kolzer M., Arenz C., Ferlinz K., Werth N., Schulze H., Klingenstein R., et al. Phosphatidylinositol-3, 5-Bisphosphate is a potent and selective inhibitor of acid sphingomyelinase. Biological Chemistry 384 (2003) 1293-1298
21. Lee P.W., Hung B.K., Woo E.K., Tai P.T., and Choi D.T. Effects of radiation therapy on neuropsychological functioning in patients with nasopharyngeal carcinoma. Journal of Neurology Neurosurg Psychiatry 52 (1989) 488-492
22. Leuner B., Mendolia-Loffredo S., Kozorovitskiy Y., Samburg D., Gould E., and Shors T.J. Learning enhances the survival of new neurons beyond the time when the hippocampus is required for memory. Journal of Neuroscience 24 (2004) 7477-7481
23. Macedoni-Luksic M., Jereb B., and Todorovski L. Long-term sequelae in children treated for brain tumors: Impairments, disability, and handicap. Pediatric Hematology and Oncology 20 (2003) 89-101
24. Madsen T.M., Kristjansen P.E., Bolwig T.G., and Wortwein G. Arrested neuronal proliferation and impaired hippocampal function following fractionated brain irradiation in the adult rat. Neuroscience 119 (2003) 635-642
25. McEchron M.D., Bouwmeester H., Tseng W., Weiss C., and Disterhoft J.F. Hippocampectomy disrupts auditory trace fear conditioning and contextual fear conditioning in the rat. Hippocampus 8 (1998) 638-646
26. 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. Nat Neurosci 9 (2006) 729-731
27. Mizumatsu S., Monje M.L., Morhardt D.R., Rola R., Palmer T.D., and Fike J.R. Extreme sensitivity of adult neurogenesis to low doses of X-irradiation. Cancer Research 63 (2003) 4021-4027
28. Monje M.L., Toda H., and Palmer T.D. Inflammatory blockade restores adult hippocampal neurogenesis. Science 302 (2003) 1760-1765
29. Nieder C., Andratschke N., Price R.E., Rivera B., and Ang K.K. Innovative prevention strategies for radiation necrosis of the central nervous system. Anticancer Research 22 (2002) 1017-1023
30. Pena L.A., Fuks Z., and Kolesnick R.N. Radiation-induced apoptosis of endothelial cells in the murine central nervous system: Protection by fibroblast growth factor and sphingomyelinase deficiency. Cancer Research 60 (2000) 321-327
31. Phillips R.G., and LeDoux J.E. Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behavioral Neuroscience 106 (1992) 274-285
32. Ramirez-Amaya V., Marrone D.F., Gage F.H., Worley P.F., and Barnes C.A. Integration of new neurons into functional neural networks. Journal of Neuroscience 26 (2006) 12237-12241
33. Rogers J.L., Hunsaker M.R., and Kesner R.P. Effects of ventral and dorsal CA1 subregional lesions on trace fear conditioning. Neurobiology of Learning and Memory 86 (2006) 72-81
34. Roman D.D., and Sperduto P.W. Neuropsychological effects of cranial radiation: Current knowledge and future directions. International Journal of Radiation Oncology, Biology, Physics 31 (1995) 983-998
35. 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 103 (2006) 17501-17506
36. Schatz J., Kramer J.H., Ablin A., and Matthay K.K. Processing speed, working memory, and IQ: A developmental model of cognitive deficits following cranial radiation therapy. Neuropsychology 14 (2000) 189-200
37. Schlessinger A.R., Cowan W.M., and Gottlieb D.I. An autoradiographic study of the time of origin and the pattern of granule cell migration in the dentate gyrus of the rat. Journal of Comparative Neurology 159 (1975) 149-175
38. Schmidt-Hieber C., Jonas P., and Bischofberger J. Enhanced synaptic plasticity in newly generated granule cells of the adult hippocampus. Nature 429 (2004) 184-187
39. Shors T.J., Miesegaes G., Beylin A., Zhao M., Rydel T., and Gould E. Neurogenesis in the adult is involved in the formation of trace memories. Nature 410 (2001) 372-376
40. Shors T.J., Townsend D.A., Zhao M., Kozorovitskiy Y., and Gould E. Neurogenesis may relate to some but not all types of hippocampal-dependent learning. Hippocampus 12 (2002) 578-584
41. Sienkiewicz Z.J., Haylock R.G., and Saunders R.D. Prenatal irradiation and spatial memory in mice: Investigation of dose-response relationship. International Journal of Radiation Biology 65 (1994) 611-618
42. Surma-aho O., Niemela M., Vilkki J., Kouri M., Brander A., Salonen O., et al. Adverse long-term effects of brain radiotherapy in adult low-grade glioma patients. Neurology 56 (2001) 1285-1290
43. Tada E., Parent J.M., Lowenstein D.H., and Fike J.R. X-irradiation causes a prolonged reduction in cell proliferation in the dentate gyrus of adult rats. Neuroscience 99 (2000) 33-41
44. Wang S., Scott B.W., and Wojtowicz J.M. Heterogenous properties of dentate granule neurons in the adult rat. Journal of Neurobiology 42 (2000) 248-257
45. Weiss C., Bouwmeester H., Power J.M., and Disterhoft J.F. Hippocampal lesions prevent trace eyeblink conditioning in the freely moving rat. Behavioural Brain Research 99 (1999) 123-132
46. Winocur G., Wojtowicz J.M., Sekeres M., Snyder J.S., and Wang S. Inhibition of neurogenesis interferes with hippocampus-dependent memory function. Hippocampus 16 (2006) 296-304
47. Zhao C., Teng E.M., Summers Jr. R.G., Ming G.L., and Gage F.H. Distinct morphological stages of dentate granule neuron maturation in the adult mouse hippocampus. Journal of Neuroscience 26 (2006) 3-11