In vivo evaluation of cellular activity in αCaMKII heterozygous knockout mice using manganese-enhanced magnetic resonance imaging (MEMRI)

Frontiers in Integrative Neuroscience

Volumn 7, Issue NOV, 2013, Pages

  Hattori, Satoko ^a,b,c   Hagihara, Hideo ^b,c   Ohira, Koji ^b,c   Aoki, Ichio ^a   Saga, Tsuneo ^a   Suhara, Tetsuya ^a   Higuchi, Makoto ^a   Miyakawa, Tsuyoshi ^b,c,d  

^a NATIONAL INSTITUTE OF RADIOLOGICAL SCIENCES   (Japan)

^b FUJITA HEALTH UNIVERSITY   (Japan)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^d NATIONAL INSTITUTE FOR PHYSIOLOGICAL SCIENCES   (Japan)

Author keywords

CaMKII; Bed nucleus of stria terminalis; Dentate gyrus; Hippocampus; Immature; Manganese enhanced MRI; Psychiatric disorder; Schizophrenia

Indexed keywords

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II ALPHA; CALCIUM CHANNEL; LIGAND GATED CALCIUM CHANNEL; MANGANESE; MANGANESE CHLORIDE; UNCLASSIFIED DRUG; VOLTAGE GATED CALCIUM CHANNEL;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ANXIETY DISORDER; ARTICLE; BRAIN NERVE CELL; BRAIN TISSUE; COGNITION; COGNITIVE DEFECT; CONTROLLED STUDY; DENTATE GYRUS; ENZYME ACTIVITY; ENZYME ANALYSIS; GLIA CELL; HIPPOCAMPAL CA1 REGION; IMAGE ENHANCEMENT; IN VIVO STUDY; ION TRANSPORT; KNOCKOUT MOUSE; MAGNET; MOUSE; MOUSE MUTANT; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SCANNER; SIGNAL PROCESSING; STRIA TERMINALIS;

EID: 84888100448     PISSN: 16625145     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnint.2013.00076     Document Type: Article

References (52)

1. Amaral, D. G., and Witter, M. P. (2003). The three-dimensional organization of the hippocampal formation: a review of anatomical data. Neuroscience 31, 571-579. doi: 10.1016/0306-4522(89)90424-7
2. Aoki, I., Wu, Y.-J. L., Silva, A. C., Lynch, R. M., and Koretsky, A. P. (2004). In vivo detection of neuroarchitecture in the rodent brain using manganese-enhanced MRI. Neuroimage 22, 1046-1059. doi: 10.1016/j.neuroimage.2004.03.031
3. Chen, C., Rainnie, D. G., Greene, R. W., and Tonegawa, S. (1994). Abnormal fear response and aggressive behavior in mutant mice deficient for alpha-calcium-calmodulin kinase II. Science 266, 291-294. doi: 10.1126/science.7939668
4. Choi, D. C., Furay, A. R., Evanson, N. K., Ostrander, M. M., Ulrich-Lai, Y. M., and Herman, J. P. (2007). Bed nucleus of the stria terminalis subregions differentially regulate hypothalamic-pituitary-adrenal axis activity: implications for the integration of limbic inputs. J. Neurosci. 27, 2025-2034. doi: 10.1523/jneurosci. 4301-06.2007
5. Elgersma, Y., Fedorov, N. B., Ikonen, S., Choi, E. S., Elgersma, M., Carvalho, O. M., et al. (2002). Inhibitory autophosphorylation of CaMKII controls PSD association, plasticity, and learning. Neuron 36, 493-505. doi: 10.1016/s0896-6273(02)01007-3
6. Elgersma, Y., Sweatt, J. D., and Giese, K. P. (2004). Mouse genetic approaches to investigating calcium/calmodulin-dependent protein kinase II function in plasticity and cognition. J. Neurosci. 24, 8410-8415. doi: 10.1523/jneurosci. 3622-04.2004
7. Emerich, D. F., and Walsh, T. J. (1989). Selective working memory impairments following intradentate injection of colchicine: attenuation of the behavioral but not the neuropathological effects by gangliosides GM1 and AGF2. Physiol. Behav. 45, 93-101. doi: 10.1016/0031-9384(89)90170-4
8. Frankland, P. W., O'Brien, C., Ohno, M., Kirkwood, A., and Silva, A. J. (2001). Alpha-CaMKII-dependent plasticity in the cortex is required for permanent memory. Nature 411, 309-313. doi: 10.1038/35077089
9. Gilbert, P. E., and Kesner, R. P. (2003). Localization of function within the dorsal hippocampus: the role of the CA3 subregion in paired-associate learning. Behav. Neurosci. 117, 1385-1394. doi: 10.1037/0735-7044.117.6.1385
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. doi: 10.1002/hipo.1077
11. Goldman-Rakic, P. S. (1994). Working memory dysfunction in schizophrenia. J. Neuropsych. Clin. Neurosci. 6, 348-357.
12. Gordon, J. A., Cioffi, D., Silva, A. J., and Stryker, M. P. (1996). Deficient plasticity in the primary visual cortex of alpha-calcium/calmodulin-dependent protein kinase II mutant mice. Neuron 17, 491-499. doi: 10.1016/s0896-6273(00)801816
13. Hagihara, H., Graef, I. A., Crabtree, G. R., and Miyakawa, T. (2011). Forebrain-specific calcineurin deficiency causes immaturity of the dentate granule cells in adult mice. Sfn meeting 2001 abstract, Available at: http://ep65.eventpilotadmin.com/web/page.php?page=IntHtml&;project=SfN12&;id=33297.
14. Hagihara, H., Takao, K., Walton, N., Matsumoto, M., and Miyakawa, T. (2013). Immature dentate gyrus: an endophenotype of neuropsychiatric disorders. Neural Plast. 2013:318596. doi: 10.1155/2013/318596
15. Hankir, M. K., Parkinson, J. R., Bloom, S. R., and Bell, J. D. (2012). The effects of glutamate receptor agonists and antagonists on mouse hypothalamic and hippocampal neuronal activity shown through manganese enhanced MRI. Neuroimage 59, 968-978. doi: 10.1016/j.neuroimage.2011.08. 063
16. Henze, D. A., Urban, N. N., and Barrionuevo, G. (2000). The multifarious hippocampal mossy fiber pathway: a review. Neuroscience 98, 407-427. doi: 10. 1016/s0306-4522(00)00146-9
17. Itoh, K., Sakata, M., Watanabe, M., Aikawa, Y., and Fujii, H. (2008). The entry of manganese ions into the brain is accelerated by the activation of N-methyl-D-aspartate receptors. Neuroscience 154, 732-740. doi: 10.1016/j.neuroscience. 2008.03.080
18. Jennings, J. H., Sparta, D. R., Stamatakis, A. M., Ung, R. L., Pleil, K. E., Kash, T. L., et al. (2013). Distinct extended amygdala circuits for divergent motivational states. Nature 496, 224-228. doi: 10.1038/nature12041
19. Kawai, Y., Aoki, I., Umeda, M., Higuchi, T., Kershaw, J., Higuchi, M., et al. (2010). In vivo visualization of reactive gliosis using manganese-enhanced magnetic resonance imaging. Neuroimage 49, 3122-3131. doi: 10.1016/j.neuroimage.2009.11. 005
20. Kim, S.-Y., Adhikari, A., Lee, S. Y., Marshel, J. H., Kim, C. K., Mallory, C. S., et al. (2013). Diverging neural pathways assemble a behavioural state from separable features in anxiety. Nature 496, 219-223. doi: 10.1038/nature 12018
21. Kobayashi, K., Ikeda, Y., Sakai, A., Yamasaki, N., Haneda, E., Miyakawa, T., et al. (2010). Reversal of hippocampal neuronal maturation by serotonergic antidepressants. Proc. Natl. Acad. Sci. U S A 107, 8434-8439. doi: 10.1073/pnas. 0912690107
22. Lacefield, C. O., Itskov, V., Reardon, T., Hen, R., and Gordon, J. A. (2012). Effects of adult-generated granule cells on coordinated network activity in the dentate gyrus. Hippocampus 22, 106-116. doi: 10.1002/hipo.20860
23. Lee, I., and Kesner, R. P. (2004a). Differential contributions of dorsal hippocampal subregions to memory acquisition and retrieval in contextual fear-conditioning. Hippocampus 14, 301-310. doi: 10.1002/hipo.10177
24. Lee, I., and Kesner, R. P. (2004b). Encoding versus retrieval of spatial memory: double dissociation between the dentate gyrus and the perforant path inputs into CA3 in the dorsal hippocampus. Hippocampus 14, 66-76. doi: 10.1002/hipo. 10167
25. Leutgeb, J. K., Leutgeb, S., Moser, M.-B., and Moser, E. I. (2007). Pattern separation in the dentate gyrus and CA3 of the hippocampus. Science 315, 961-966. doi: 10. 1126/science.1135801
26. Lisman, J., Schulman, H., and Cline, H. (2002). The molecular basis of CaMKII function in synaptic and behavioural memory. Nat. Rev. Neurosci. 3, 175-190. doi: 10.1038/nrn753
27. Lutkenhoff, E., Karlsgodt, K. H., Gutman, B., Stein, J. L., Thompson, P. M., Cannon, T. D., et al. (2012). Structural and functional neuroimaging phenotypes in dysbindin mutant mice. Neuroimage 62, 120-129. doi: 10.1016/j.neuroimage. 2012.05.008
28. Matsuo, N., Yamasaki, N., Ohira, K., Takao, K., Toyama, K., Eguchi, M., et al. (2009). Neural activity changes underlying the working memory deficit in alpha-CaMKII heterozygous knockout mice. Front. Behav. Neurosci. 3:20. doi: 10.3389/neuro.08.020.2009
29. McHugh, T. J., Jones, M. W., Quinn, J. J., Balthasar, N., Coppari, R., Elmquist, J. K., et al. (2007). Dentate gyrus NMDA receptors mediate rapid pattern separation in the hippocampal network. Science 317, 94-99. doi: 10.1126/science.1140263
30. McLamb, R. L., Mundy, W. R., and Tilson, H. A. (1988). Intradentate colchicines disrupts the acquisition and performance of a working memory task in the radial arm maze. Neurotoxicology 9, 521-528.
31. Morita, H., Ogino, T., Seo, Y., Fujiki, N., Tanaka, K., Takamata, A., et al. (2002). Detection of hypothalamic activation by manganese ion contrasted T(1)-weighted magnetic resonance imaging in rats. Neurosci. Lett. 326, 101-104. doi: 10.1016/s0304-3940(02)00330-0
32. Morris, A. M., Churchwell, J. C., Kesner, R. P., and Gilbert, P. E. (2012). Selective lesions of the dentate gyrus produce disruptions in place learning for adjacent spatial locations. Neurobiol. Learn. Mem. 97, 326-331. doi: 10.1016/j.nlm.2012. 02.005
33. Nakashiba, T., Young, J. Z., McHugh, T. J., Buhl, D. L., and Tonegawa, S. (2008). Transgenic inhibition of synaptic transmission reveals role of CA3 output in hippocampal learning. Science 319, 1260-1264. doi: 10.1126/science.1151120
34. Novak, G., and Seeman, P. (2010). Hyperactive mice show elevated D2(High) receptors, a model for schizophrenia: calcium/calmodulin-dependent kinase II alpha knockouts. Synapse 64, 794-800. doi: 10.1002/syn.20786
35. Ohira, K., Kobayashi, K., Toyama, K., Nakamura, H. K., Shoji, H., Takao, K., et al. (2013). Synaptosomal-associated protein 25 mutation induces immaturity of the dentate granule cells of adult mice. Mol. Brain 6:12. doi: 10.1186/1756-6606-6-12
36. Paxinos, D. G., and Franklin, K. B. J. (2001). The Mouse Brain in Stereotaxic Coordinates: Compact. 2nd Edn. San Diego, California, USA: Academic Press.
37. Perez, P. D., Hall, G., Kimura, T., Ren, Y., Bailey, R. M., Lewis, J., et al. (2013). In vivo functional brain mapping in a conditional mouse model of human tauopathy (tau(P301L)) reveals reduced neural activity in memory formation structures. Mol. Neurodegener. 8:9. doi: 10.1186/1750-1326-8-9
38. Schobel, S. A., Lewandowski, N. M., Corcoran, C. M., Moore, H., Brown, T., Malaspina, D., et al. (2009). Differential targeting of the CA1 subfield of the hippocampal formation by schizophrenia and related psychotic disorders. Arch. Gen. Psychiat. 66, 938-946. doi: 10.1001/archgenpsychiatry.2009.115
39. Shin, R., Kobayashi, K., Hagihara, H., Kogan, J. H., Miyake, S., Tajinda, K., et al. (2013). The immature dentate gyrus represents a shared phenotype of mouse models of epilepsy and psychiatric disease. Bipolar Disord. doi: 10.1111/bdi. 12064. [Epub ahead of print].
40. Silva, A. C., and Bock, N. A. (2008). Manganese-enhanced MRI: an exceptional tool in translational neuroimaging. Schizophr. Bull. 34, 595-604. doi: 10. 1093/schbul/sbn056
41. Silva, A. C., Lee, J. H., Aoki, I., and Koretsky, A. P. (2004). Manganese-enhanced magnetic resonance imaging (MEMRI): methodological and practical considerations. NMR Biomed. 17, 532-543. doi: 10.1002/nbm.945
42. Silva, A. J., Paylor, R., Wehner, J. M., and Tonegawa, S. (1992). Impaired spatial learning in alpha-calcium-calmodulin kinase II mutant mice. Science 257, 206-211. doi: 10.1126/science.1321493
43. Silva, A. J., Rosahl, T. W., Chapman, P. F., Marowitz, Z., Friedman, E., Frankland, P. W., et al. (1996). Impaired learning in mice with abnormal short-lived plasticity. Curr. Biol. 6, 1509-1518. doi: 10.1016/s0960-9822(96)00756-7
44. Song, J., Christian, K. M., Ming, G., and Song, H. (2012). Modification of hippocampal circuitry by adult neurogenesis. Dev. Neurobiol. 72, 1032-1043. doi: 10.1002/dneu.22014
45. Takao, K., Kobayashi, K., Hagihara, H., Ohira, K., Shoji, H., Hattori, S., et al. (2013). Deficiency of schnurri-2, an MHC enhancer binding protein, induces mild chronic inflammation in the brain and confers molecular, neuronal, and behavioral phenotypes related to schizophrenia. Neuropsychopharmacology 38, 1409-1425. doi: 10.1038/npp.2013.38
46. Tamminga, C. A., Stan, A. D., and Wagner, A. D. (2010). The hippocampal formation in schizophrenia. Am. J. Psychiat. 167, 1178-1193. doi: 10.1176/appi. ajp.2010.09081187
47. Walton, N. M., Zhou, Y., Kogan, J. H., Shin, R., Webster, M., Gross, A. K., et al. (2012). Detection of an immature dentate gyrus feature in human schizophrenia/bipolar patients. Transl. Psychiat. 2:e135. doi: 10.1038/tp.2012. 56
48. Watanabe, T., Michaelis, T., and Frahm, J. (2001). Mapping of retinal projections in the living rat using high-resolution 3D gradient-echo MRI with Mn2+-induced contrast. Magn. Reson. Med. 46, 424-429. doi: 10.1002/mrm. 1209
49. Widerøe, M., Olsen, Ø., Pedersen, T. B., Goa, P. E., Kavelaars, A., Heijnen, C., et al. (2009). Manganese-enhanced magnetic resonance imaging of hypoxicischemic brain injury in the neonatal rat. Neuroimage 45, 880-890. doi: 10. 1016/j.neuroimage.2008.12.007
50. Yamasaki, N., Maekawa, M., Kobayashi, K., Kajii, Y., Maeda, J., Soma, M., et al. (2008). Alpha-CaMKII deficiency causes immature dentate gyrus, a novel candidate endophenotype of psychiatric disorders. Mol. Brain 1:6. doi: 10. 1186/1756-6606-1-6
51. Yassa, M. A., Hazlett, R. L., Stark, C. E. L., and Hoehn-Saric, R. (2012). Functional MRI of the amygdala and bed nucleus of the stria terminalis during conditions of uncertainty in generalized anxiety disorder. J. Psychiatr. Res. 46, 1045-1052. doi: 10.1016/j.jpsychires.2012.04.013
52. Yu, X., Wadghiri, Y. Z., Sanes, D. H., and Turnbull, D. H. (2005). In vivo auditory brain mapping in mice with Mn-enhanced MRI. Nat. Neurosci. 8, 961-968. doi: 10.1038/nn1477