Three axonal projection routes of individual pyramidal cells in the ventral CA1 hippocampus

Frontiers in Neuroanatomy

Volumn 8, Issue JUN, 2014, Pages

  Arszovszki, Antónia ^a   Borhegyi, Zsolt ^a   Klausberger, Thomas ^a,b  

^a Medical University of Vienna   (Austria)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Apical dendrite; Axonal projection; Calbindin; Norbin; Pyramidal neuron; Ventral CA1

Indexed keywords

CALBINDIN; NEUROTRANSMITTER;

ADULT; ANATOMICAL CONCEPTS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DENDRITE; ELECTROCARDIOGRAPHY; ELECTRON MICROSCOPY; HEMISPHERE; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA2 REGION; HIPPOCAMPAL CA3 REGION; IMMUNOHISTOCHEMISTRY; MALE; NERVE FIBER MEMBRANE; NONHUMAN; PYRAMIDAL NERVE CELL; RAT;

EID: 84929460026     PISSN: None     EISSN: 16625129     Source Type: Journal    
DOI: 10.3389/fnana.2014.00053     Document Type: Article

References (55)

1. Airaksinen, M. S., Eilers, J., Garaschuk, O., Thoenen, H., Konnerth, A., and Meyer, M. (1997). Ataxia and altered dendritic calcium signaling in mice carrying a targeted null mutation of the calbindin D28k gene. Proc. Natl. Acad. Sci. U.S.A. 94, 1488-1493. doi: 10.1073/pnas.94.4.1488
2. Amaral, D. G., Dolorfo, C., andAlvarez-Royo, P. (1991). Organization of CA1 projections to the subiculum: a PHA-L analysis in the rat. Hippocampus 1, 415-435. doi: 10.1002/hipo.450010410
3. Amaral, D. G., and Lavenex, P. (2007). "Hippocampal neuroanatomy," in The Hippocampus Book, eds P. Andersen, R. Morris, D. Amaral, T. Bliss, and J. O'Keefe (NewYork, NY: Oxford UniversityPress), 872.
4. Amaral, D. G., andWitter, M. P. (1989). The three-dimensional organization of the hippocampal formation: areviewof anatomical data. Neuroscience 31, 571-591. doi: 10.1016/0306-4522(89)90424-7
5. Andersen, P., Bliss, T. V., and Skrede, K. K. (1971). Lamellar organization of hippocampal pathways. Exp. Brain Res. 13, 222-238. doi: 10.1007/BF00234087
6. Baimbridge, K. G., and Miller, J. J. (1982). Immunohistochemical localization of calcium-binding protein in the cerebellum, hippocampal formation and olfactory bulb of the rat. Brain Res. 245, 223-229. doi: 10.1016/0006-8993(82) 90804-6
7. Baimbridge, K. G., Peet, M. J., McLennan, H., and Church, J. (1991). Bursting response to current-evoked depolarization in rat CA1 pyramidal neurons is correlated with lucifer yellow dye coupling but not the presence of calbindin-D28k. Synapse 360, 150-160.
8. Bannerman, D. M., Deacon, R. M., Offen, S., Friswell, J., Grubb, M., and Rawlins, J. N. (2002). Double dissociation of function within the hippocampus: spatial memoryandhyponeophagia. Behav. Neurosci. 116, 884-901. doi: 10.1037/07357044.116.5.884
9. Bannerman, D. M., Rawlins, J. N., McHugh, S. B., Deacon, R. M., Yee, B. K., Bast, T., et al. (2004). Regional dissociations within the hippocampus-memory and anxiety. Neurosci. Biobehav. Rev. 28, 273-283. doi: 10.1016/j.neubiorev.2004. 03.004
10. Bannerman, D. M., Yee, B. K., Good, M. A., Heupel, M. J., Iversen, S. D., and Rawlins, J. N. (1999). Double dissociation of function within the hippocampus: a comparison of dorsal, ventral, and complete hippocampal cytotoxic lesions. Behav. Neurosci. 113, 1170-1188. doi: 10.1037/0735-7044.113.6.1170
11. Bannister, N. J., and Larkman, A. U. (1995). Dendritic morphology of CA1 pyramidal neurones from the rat hippocampus: I. branching patterns. J. Comp. Neurol. 360, 150-160. doi: 10.1002/cne.903600111
12. Bliss, T.V., and Collingridge, G. L. (1993).Asynaptic model ofmemory: long-term potentiation in the hippocampus. Nature 361, 31-39. doi: 10.1038/361031a0
13. Bullis, J. B., Jones, T. D., and Poolos, N. P. (2007). Reversed somatodendritic I(h) gradient in a class of rat hippocampal neurons with pyramidal morphology. J. Physiol. 579, 431-443. doi: 10.1113/jphysiol.2006.123836
14. Canteras, N. S., and Swanson, L. W. (1992). Projections of the ventral subicu- lum to the amygdala, septum, and hypothalamus: a PHAL anterograde tract- tracing study in the rat. J. Comp. Neurol. 324, 180-194. doi: 10.1002/cne. 903240204
15. Celio, M. R. (1990). Calbindin D-28k and parvalbumin in the rat nervous system. Neuroscience 35, 375-475. doi: 10.1016/0306-4522(90)90091-H
16. Celio, M. R., Baier, W., Scharer, L., Gregersen, H. J., De Viragh, P. A., and Norman, A. W. (1990). Monoclonal antibodies directed against the calcium binding protein Calbindin D-28k. Cell Calcium 11, 599-602. doi: 10.1016/0143- 4160(90)90014-L
17. Cenquizca, L. A., and Swanson, L. W. (2006). Analysis of direct hippocampal cortical field CA1 axonal projections to diencephalon in the rat. J. Comp. Neurol. 497, 101-114. doi: 10.1002/cne.20985
18. Cenquizca, L. A., and Swanson, L. W. (2007). Spatial organization of direct hippocampal field CA1 axonal projections to the rest of the cerebral cortex. Brain Res. Rev. 56, 1-26. doi: 10.1016/j.brainresrev.2007.05.002
19. Dateki, M., Horii, T., Kasuya, Y., Mochizuki, R., Nagao, Y., Ishida, J., et al. (2005). Neurochondrin negatively regulates CAMKII phosphorylation, and nervous system-specific gene disruption results in epileptic seizure. J. Biol. Chem. 280, 20503-20508. doi: 10.1074/jbc.M414033200
20. Dolorfo, C. L., andAmaral, D. G. (1998). Entorhinal cortex of the rat: topographic organization of the cells of origin of the perforant path projection to the dentate gyrus. J. Comp. Neurol. 398, 25-48.
21. Dong, H. W., Swanson, L. W., Chen, L., Fanselow, M. S., and Toga, A. W. (2009). Genomic-anatomic evidence for distinct functional domains in hippocampal field CA1. Proc. Natl. Acad. Sci. U.S.A. 106, 11794-11799. doi: 10.1073/pnas. 0812608106
22. Eichenbaum, H. (1999). The hippocampus and mechanisms of declarative memory. Behav. Brain Res. 103, 123-133. doi: 10.1016/S0166-4328(99) 00044-3
23. Graves, A. R., Moore, S. J., Bloss, E. B., Mensh, B. D., Kath, W. L., and Spruston, N. (2012). Hippocampal pyramidal neurons comprise two distinct cell types that are countermodulatedbymetabotropic receptors. Neuron 76, 776-789. doi: 10.1016/j.neuron.2012.09.036
24. Gulyas, A. I., Toth, K., McBain, C. J., and Freund, T. F. (1998). Stratum radiatum giant cells: a type of principal cell in the rat hippocampus. Eur. J. Neurosci. 10, 3813-3822. doi: 10.1046/j.1460-9568.1998.00402.x
25. Harris, E., Witter, M. P., Weinstein, G., and Stewart, M. (2001). Intrinsic connectivity of the rat subiculum: i. dendritic morphology and patterns of axonal arborization by pyramidal neurons. J. Comp. Neurol. 435, 490-505. doi: 10.1002/cne.1046
26. Ishikawa, A., and Nakamura, S. (2006). Ventral hippocampal neurons project axons simultaneously to the medial prefrontal cortex and amygdala in the rat. J. Neurophysiol. 96,2134-2138. doi: 10.1152/jn.00069.2006
27. Istvanffy, R., Vogt Weisenhorn, D. M., Floss, T., and Wurst, W. (2004). Expression of neurochondrin in the developing and adult mouse brain. Dev. Genes Evol. 214, 206-209. doi: 10.1007/s00427-004-0396-2
28. Jung, M. W., Wiener, S. I., and McNaughton, B. L. (1994). Comparison of spatial firing characteristics of units in dorsal and ventral hippocampus of the rat. J. Neurosci. 14, 7347-7356.
29. Kjelstrup, K. B., Solstad, T., Brun, V. H., Hafting, T., Leutgeb, S., Witter, M. P., et al. (2008). Finite scale of spatial representation in the hippocampus. Science 321, 140-143. doi: 10.1126/science.1157086
30. Klausberger, T., and Somogyi, P. (2008). Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations. Science 321, 53-57. doi: 10.1126/science.1149381
31. Lorente De No, R. (1934). Studies on the structure of the cerebral cortex. II. Continuation of the study of the ammonic system. J. Psychol. Neurol. 46, 113-177.
32. Losonczy, A., Zhang, L., Shigemoto, R., Somogyi, P., and Nusser, Z. (2002). Cell type dependence and variability in the short-term plasticity of EPSCs in identified mouse hippocampal interneurones. J. Physiol. 542, 193-210. doi: 10.1113/jphysiol.2002.020024
33. Maccaferri, G., and McBain, C. J. (1996). Long-term potentiation in distinct subtypes ofhippocampal nonpyramidal neurons. J. Neurosci. 16, 5334-5343.
34. Mizuseki, K., Diba, K., Pastalkova, E., and Buzsaki, G. (2011). Hippocampal CA1 pyramidal cells form functionally distinct sublayers. Nat. Neurosci. 14, 1174-1181. doi: 10.1038/nn.2894
35. Molinari, S., Battini, R., Ferrari, S., Pozzi, L., Kilcross, A. S., Robbins, T. W., et al. (1996). Deficits in memory and hippocampal long-term potenciation in mice with reduced calbindin D28K expression. Proc. Natl. Acad. Sci. U.S.A. 15, 8028-8033. doi: 10.1073/pnas.93.15.8028
36. Moser, M. B., and Moser, E. I. (1998). Functional differentiation in the hippocampus. Hippocampus 8, 608-619.
37. Moser, M. B., Moser, E. I., Forrest, E., Andersen, P., and Morris, R. G (1995). Spatial learningwith aminislab in the dorsal hippocampus. Proc. Natl. Acad. Sci. U.S.A. 92, 9697-9701. doi: 10.1073/pnas.92.21.9697
38. O'keefe, J. (1976). Place units in the hippocampus of the freely moving rat. Exp. Neurol. 51, 78-109. doi: 10.1016/0014-4886(76)90055-8
39. Paxinos, G., and Watson, C. (2007). The Rat Brain in Stereotaxic Coordinates, 6th Edn. San Diego, CA: Elsevier Academic Press.
40. Pinault, D. (1996). A novel single-cell staining procedure performed in vivo under electrophysiological control: morpho-functional features of juxtacellu- larlylabeled thalamic cells and other central neurons with biocytin or neurobiotin. J. Neurosci. Methods 65, 113-136. doi: 10.1016/0165-0270(95)00144-1
41. Rami, A., Brehier, A., Thomasset, M., and Rabie, A. (1987). The comparative immunocytochemical distribution of 28 kDa cholecalcin (CaBP) in the hippocampus of rat, guinea pig and hedgehog. Brain Res. 422, 149-153. doi: 10.1016/0006-8993(87)90549-X
42. Ratzliff, A. D., and Soltesz, I. (2001). Differential immunoreactivity for alpha-actinin-2, an N-methyl-D-aspartate-receptor/actin binding protein, in hippocampal interneurons. Neuroscience 103, 337-349. doi: 10.1016/S0306- 4522(01)00013-6
43. Risold, P. Y., and Swanson, L. W. (1996). Structural evidence for functional domains in the rat hippocampus. Science 272, 1484-1486. doi: 10.1126/sci- ence.272.5267.1484
44. Shinozaki, K., Kume, H., Kuzume, H., Obata, K., and Maruyama, K. (1999). Norbin, a neurite-outgrowth-related protein, is a cytosolic protein localized in the somatodendritic region of neurons and distributed prominently in dendritic outgrowth in purkinje cells. Brain Res. Mol. Brain Res. 71, 364-368. doi: 10.1016/S0169-328X(99)00181-3
45. Sloviter, R. S. (1989). Calcium-binding protein (calbindin-D28k) and parvalbumin immunocytochemistry: localization in the rat hippocampus with specific reference to the selective vulnerability of hippocampal neurons to seizure activity. J. Comp. Neurol. 280, 183-196. doi: 10.1002/cne.902800203
46. Spruston, N. (2008). Pyramidal neurons: dendritic structure and synaptic integration. Nat. Rev. Neurosci. 9, 206-221. doi: 10.1038/nrn2286
47. Squire, L. R. (2007). "Memory systems: a biological concept," in Science of Memory: Concepts, eds R. Roediger, Y. Dudai, and S. Fitzpatrick (Oxford: Oxford University Press), 339-343.
48. Swanson, L. W. (2004). Brain Maps: Structure of the Rat Brain. San Diego, CA: Elsevier Academic Press.
49. Swanson, L. W., and Cowan, W. M. (1977). An autoradiographic study of the organization of the efferent connections of the hippocampal formation in the rat. J. Comp. Neurol. 172, 49-84. doi: 10.1002/cne.901720104
50. Tamamaki, N., Abe, K., and Nojyo, Y. (1987). Columnar organization in the subiculum formed by axon branches originating from single CA1 pyramidal neurons in the rat hippocampus. Brain Res. 412, 156-160. doi: 10.1016/0006- 8993(87)91452-1
51. Tamamaki, N., and Nojyo, Y. (1991). Crossing fiber arrays in the rat hippocampus as demonstrated by three-dimensional reconstruction. J. Comp. Neurol. 303, 435-442. doi: 10.1002/cne.903030309
52. Van Groen, T., and Wyss, J. M. (1990). Extrinsic projections from area CA1 of the rat hippocampus: olfactory, cortical, subcortical, and bilateral hippocampal formation projections. J. Comp. Neurol. 302, 515-528. doi: 10.1002/cne.9030 20308
53. Wang, H., Westin, Y. N., Birnbaum, S., Bendor, J., Brismar, H., Nestler, E., et al. (2009). Norbin is an endogenous regulator of metabotropic glutamate receptor 5 signaling. Science 326, 1554-1557. doi: 10.1126/science.1178496
54. Witter, M. P., and Amaral, D. G. (2004). "Hippocampal formation," in The Rat Nervous System, ed G. Paxinos (Amsterdam: Elsevier), 637-703.
55. Zhou, R. (1997). Regulation of topographic projection by the Eph family receptor Bsk (EphA5) and its ligands. Cell Tissue Res. 290, 251-259. doi: 10.1007/s004410050929