Pyramidal neurons in the septal and temporal CA1 field of the human and hedgehog tenrec hippocampus

Brain Research

Volumn 1218, Issue , 2008, Pages 35-46

  Liagkouras, Ioannis ^a   Michaloudi, Helen ^a   Batzios, Christos ^a   Psaroulis, Dimitrios ^a   Georgiadis, Marios ^a   Künzle, Heinz ^b   Papadopoulos, Georgios C ^a  

^a ARISTOTLE UNIVERSITY OF THESSALONIKI   (Greece)

^b UNIVERSITY OF MUNICH   (Germany)

Author keywords

Cell density; Dendrites; Disector method; Rapid Golgi method; Septotemporal differentiation; Spines

Indexed keywords

ARTICLE; CELL DENSITY; DENDRITIC CELL; HEDGEHOG; HEMISPHERE; HIPPOCAMPUS; HUMAN; HUMAN CELL; MORPHOMETRICS; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SEPTUM PELLUCIDUM; TEMPORAL CORTEX;

ADULT; ANIMALS; DENDRITES; FEMALE; HEDGEHOGS; HIPPOCAMPUS; HUMANS; MALE; MIDDLE AGED; MODELS, NEUROLOGICAL; PYRAMIDAL CELLS; SILVER STAINING; SPECIES SPECIFICITY;

ERINACEIDAE; TENREC;

EID: 46349103881     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2008.04.037     Document Type: Article

References (116)

1. Aihara H., Li X., Fujiwara S., Matsumura T., Okumura S., Tozaki H., Kanno T., Ohta K., Nagai K., and Nishizaki T. The protective action of nefiracetam against electrophysiological and metabolic damage in the hippocampus after deprivation of glucose and oxygen. Brain Res. 922 (2001) 58-162
2. Akaike K., Tanaka S., Tojo H., Fukumoto S., Imamura S., and Takigawa M. Kainic acid-induced dorsal and ventral hippocampal seizures in rats. Brain Res. 900 (2001) 65-71
3. Amaral D.G., and Witter M.P. The three-dimensional organization of the hippocampal formation: a review of anatomical data. Neuroscience 31 (1989) 571-591
4. Amaral D., Insausti R., and Cowan W. The commissural connection of the monkey hippocampal formation. J. Comp. Neurol. 224 (1984) 307-336
5. Ashton D., Reempts J.V., Haseldonckx M., and Willems R. Dorsal-ventral gradient in vulnerability of CA1 hippocampus to ischemia: a combined histological and electrophysiological study. Brain Res. 487 (1989) 368-372
6. Babb T.L., Brown W.J., Pretorius J., Davenport C., Lieb J.P., and Crandall P.H. Temporal lobe and volumetric cell densities in temporal lobe epilepsy. Epilepsia 25 (1984) 729-740
7. Bancroft A., and Levin E.D. Ventral hippocampal a4β2 nicotinic receptors and chronic nicotine effects on memory. Neuropharmacology 39 (2000) 2770-2778
8. Becker A., Letzel K., Letzel U., and Grecksch G. Kindling of the dorsal and the ventral hippocampus: effects on learning performance in rats. Physiol. Behav. 62 (1997) 1265-1271
9. Borck C., and Jefferys J.G. Seizure-like events in disinhibited ventral slices of adult rat hippocampus. J. Neurophysiol. 82 (1999) 2130-2142
10. Bragdon A.C., Taylor D.M., and Wilson W.A. Potassium-induced epileptiform activity in area CA3 varies markedly along the septotemporal axis of the rat hippocampus. Brain Res. 378 (1986) 169-173
11. Buckmaster P., and Amaral D. Intracellular recording and labeling of mossy cells and proximal CA3 pyramidal cells in macaque B monkeys. J. Comp. Neurol. 430 (2001) 264-281
12. Buhl E.H., and Dann J.F. Cytoarchitecture, neuronal composition, and entorhinal afferents of the flying fox hippocampus. Hippocampus 1 (1991) 131-152
13. Buzsaki G. The hippocampo-neocortical dialogue. Cereb. Cortex 6 (1996) 81-92
14. Carnevale N.T., Tsai K.Y., Claiborne B.J., and Brown T.H. Comparative electrotonic analysis of three classes of rat hippocampal neurons. Am. Physiol. Soc. (1997) 703-720
15. Cassell M.D., and Brown M.W. The distribution of Timm's Stain in the nonsulphide-perfused human hippocampal formation. J. Comp. Neurol. 222 (1984) 461-471
16. Chen H.-X., Otmakhov N., and Lisman J. Requirements for LTP induction by pairing in hippocampal CA1 pyramidal cells. Am. Physiol. Soc. (1999) 526-532
17. 2+ influx. J. Neurophysiol. 73 (1995) 2553-2557
18. Coggeshall R.E., Chung K., Greenwood D., and Hulsebosch C.E. An empirical method for converting nucleolar counts to neuronal numbers. J. Neurosci. Methods 12 (1984) 125-132
19. Crutcher K.A., Danscher G., and Geneser F.A. Hippocampus and dentate area of the european hedgehog, comparative histochemical study. Brain Behav. Evol. 32 (1988) 269-276
20. De Bow S.B., and Colbourne F. Delayed transient ischemic attacks kill some CA1 neurons previously salvaged with postischemic hypothermia: neuroprotection undone. Brain Res. 959 (2003) 50-57
21. Derchansky M., Shahar E., Wennberg R.A., Samoilova M., Jahromi S.S., Abdelmalik P.A., Zhang L., and Carlen P.L. Model of frequent, recurrent, and spontaneous seizures in the intact mouse hippocampus. Hippocampus 14 (2004) 935-947
22. Dolorfo C.L., and Amaral D.G. 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 (1998) 25-48
23. Dolorfo C.L., and Amaral D.G. Entorhinal cortex of the rat: organization of intrinsic connections. J. Comp. Neurol. 398 (1998) 49-82
24. Dominguez M.-I., Blasco-Ibanez J.M., Crespo C., Marques-Mari A.-I., and Martinez-Guijarro F.J. Calretinin/PSA-NCAM immunoreactive granule cells after hippocampal damage produced by kainic acid and DEDTC treatment in mouse. Brain Res. 966 (2003) 206-217
25. Dominguez M.-I., Blasco-Ibanez J.M., Crespo C., Marques-Mari A.-I., and Martinez-Guijarro F.J. Zinc chelation during non-lesioning overexcitation results in neuronal death in the mouse hippocampus. Neuroscience 116 (2003) 791-806
26. Dubrovsky B., Tatarinov A., Gijsbers K., Harris J., and Tsiodras A. Effects of arginine-vasopressin (AVP) on long-term potentiation in intact anesthetized rats. Brain Res. Bull. 59 (2003) 467-472
27. Dun N.J., Dun S.L., Wong R.K.S., and Forstermann U. Colocalization of nitric oxide synthetase and somatostatin immunoreactivity in rat dentate hilar neurons. Proc. Natl. Acad. Sci. U. S. A. 91 (1994) 2955-2959
28. Ferbinteanu J., and McDonald R.J. Dorsal/ventral hippocampus, fornix and conditioned place preference. Hippocampus 11 (2001) 187-200
29. Fernandez N., Andreasen M., and Nedergaard S. Influence of the hyperpolarization-activated cation current, I(h), on the electrotonic properties of the distal apical dendrites of hippocampal CA1 pyramidal neurons. Brain Res. 930 (2002) 42-52
30. Fumoto N., Nakatsuka H., Ohta S., Kumon Y., and Ohnishi T. Hippocampal CA1 neuron survival and cytosolic FKBP12, the 12kDaFK506-binding protein, after ischemia and tacrolimus treatment in gerbils. Neurosci. Lett. 339 (2003) 219-222
31. Gaarskjaer F.B., Danscher G., and West M.J. Hippocampal mossy fibers in regio superior of the European hedgehog. Brain Res. 237 (1982) 79-90
32. Gilbert M., Racine R.J., and Smith G.K. Epileptiform burst responses in ventral vs dorsal hippocampal slices. Brain Res. 361 (1985) 389-391
33. Grivas I., Michaloudi H., Batzios Ch., Chiotelli M., Papatheodoropoulos C., Kostopoulos G., and Papadopoulos G.C. Vascular network of the rat hippocampus is not homogeneous along the septotemporal axis. Brain Res. 971 (2003) 245-249
34. Gulyas A.I., Megias M., Emri Z., and Freund T.F. Total number and ratio of excitatory and inhibitory synapses converging onto single interneurons of different types in the CA1 area of the rat hippocampus. J. Neurosci. 19 (1999) 10082-10097
35. Gurr E. Staining animal tissues Practical and Theoretical (1962), Leonard Hill Books, London
36. Hertz L. Features of astrocytic function apparently involved in the response of central nervous tissue to ischemia/hypoxia. J. Cereb. Blood Flow Metab. 1 (1981) 143-153
37. Hock B.J., and Bunsey M.D. Differential effects of dorsal and ventral hippocampal lesions. J. Neurosci. 18 (1998) 7027-7032
38. Howe M.L., and Courage M.L. On resolving the enigma of infantile amnesia. Psychol. Bull. 113 (1993) 305-326
39. Izumi Y., Benz A.M., Katsuki H., Matsukawa M., Clifford D.B., and Zorumski C.F. Effects of fructose-1,6-bisphosphate on morphological and functional neuronal integrity in rat hippocampal slices during energy deprivation. Neuroscience 116 (2003) 465-475
40. Jung M.W., Wiener S.I., and McNaughton B.L. Comparison of spatial firing characteristics of units in dorsal and ventral hippocampus of the rat. J. Neurosci. 14 (1994) 7347-7356
41. Kaibara T., and Leung L.S. Basal versus apical dendritic long-term potentiation of commisural afferents to hippocampal CA1: a current-source density study. J. Neurosci. 13 (1993) 2391-2404
42. Kloosterman F., Peloquin P., and Leung L.S. Apical and basal orthodromic population spikes in hippocampal CA1 in vivo show different origins and patterns of propagation. J. Neurophysiol. 86 (2001) 2435-2444
43. Kobayashi T., Tran A.H., Nishijo H., Ono T., and Matsumoto G. Contribution of hippocampal place cell activity to learning and formation of goal-directed navigation in rats. Neuroscience 117 (2003) 1025-1035
44. Kuffler S.W., and Potter D.D. Glia in the leech central nervous system: physiological properties and neuron-glia relationship. J. Neurophysiol. 27 (1964) 290-320
45. Künzle H. Regional and laminar distribution of cortical neurons projecting to either superior or inferior colliculus in the hedgehog tenrec. Cereb. Cortex 5 (1995) 338-352
46. Künzle H., and Radtke-Schuller S. Hippocampal fields in the hedgehog tenrec. Their architecture and major intrinsic connections. Neurosci. Res. 41 (2001) 267-291
47. Lancelot E., and Beal M.F. Glutamate toxicity in chronic neurodegenerative disease. Prog. Brain Res. 116 (1998) 331-347
48. Laurberg S., and Zimmer J. Aberrant hippocampal mossy fibers in cats. Brain Res. 188 (1980) 555-559
49. Lee K.S., Reddington M., Schubert P., and Kreutzberg G. Regulation of the strength of adenosine modulation in the hippocampus by a differential distribution of the density of A1 receptors. Brain Res. 260 (1983) 156-159
50. Lee P.H., Xie C.W., Lewis D.V., Wilson W.A., Mitchell C.L., and Hong J.S. Opioid-induced epileptiform bursting in hippocampal slices: higher susceptibility in ventral than dorsal hippocampus. J. Pharmacol. Exp. Ther. 253 (1990) 545-551
51. Lim C., Blume H., Madsen J., and Saper C. Connections of the hippocampal formation in humans: I. The mossy fiber pathway. J. Comp. Neurol. 385 (1997) 325-351
52. + channels amplify EPSPs in hippocampal CA1 pyramidal cells. J. Neurophysiol. 76 (1996) 2181-2191
53. Lothman E.W., and Collins R.C. Kainic acid induced limbic seizures: metabolic, behavioral, electroencephalographic and neuropathological correlates. Brain Res. 218 (1981) 299-318
54. Ma L., Carter R.J., Morton A.J., and Nicholson L.F.B. RAGE is expressed in pyramidal cells of the hippocampus following moderate hypoxic-ischemic brain injury in rats. Brain Res. 966 (2003) 167-174
55. Mainen Z.F., and Sejnowski T.J. Influence of dendritic structure on firing pattern in model neocortical neurons. Nature 382 (1996) 363-366
56. Manschot S.M., Biessels G.-J., Cameron N.E., Cotter M.A., Kamal A., Kappelle L.J., and Gispen W.H. Angiotensin converting enzyme inhibition partially prevents deficits in water maze performance, hippocampal plasticity and cerebral blood flow in streptozotocin-diabetic rats. Brain Res. 966 (2003) 274-282
57. Markowitsch H.J. Which brain regions are critically involved in the retrieval of old episodic memory?. Brain Res. Rev. 21 (1995) 117-127
58. Maruki K., Izaki Y., Nomura M., and Yamauchi T. Differences in paired-pulse facilitation and long-term potentiation between dorsal and ventral CA1 regions in anesthetized rats. Hippocampus 11 (2001) 655-661
59. Matsuzaki H., Tamatani M., Yamaguchi A., Namikawa K., Kiyama H., Vitek M.P., Mitsuda N., and Tohyama M. Vascular endothelial growth factor rescues hippocampal neurons from glutamate-induced toxicity: signal transduction cascades. FASEB J. 15 (2001) 1218-1220
60. Megias M., Emri Z.S., Freund T.F., and Gulyas A.I. Total number and distribution of inhibitory and excitatory synapses on hippocampal CA1 pyramidal cells. Neuroscience 102 (2001) 527-540
61. Moddel G., Jacobson B., Ying Z., Janigro D., Bingaman W., Gonzalez-Martinez J., Kellinghaus C., Prayson R.A., and Najm I.M. The NMDA receptor NR2B subunit to epileptogenesis in human cortical dysplasia. Brain Res. 1046 (2005) 10-23
62. Moser M.B., and Moser E.I. Functional differentiation in the hippocampus. Hippocampus 8 (1998) 608-619
63. Moser M.B., Moser E.I., Forrest E., Andersen P., and Morris R.G.M. Spatial learning with a minislab in the dorsal hippocampus. Proc. Natl. Acad. Sci. U. S. A. 92 (1995) 9697-9701
64. Muller R.U., and Kubie J.L. The effects of changes in the environment on the spatial firing of hippocampal complex-spike cells. J. Neurosci. 7 (1987) 1951-1968
65. Nishihara H., Satta Y., Nikaido M., Thewissen J.G.M., Stanhope M.J., and Okada N. A retroposon analysis of afrotherian phylogeny. Mol. Biol. Evol. 22 (2005) 1823-1833
66. 2+ signaling in dendrites. Neuron 46 (2005) 609-622
67. Nomura T., Fukuda T., Aika Y., Heizmann C.W., Emson P.C., Kobayashi T., and Kosaka T. Laminar distribution of nonprincipal neurons in the rat hippocampus, with special reference to their dorsoventral difference. Brain Res. 751 (1997) 64-80
68. Okada T., Yamada N., Tsuzuki K., Horikawa H.P.M., Tanaka K., and Ozawa S. Long-term potentiation in the hippocampal CA1 area and dentate gyrus plays different roles in spatial learning. Eur. J. Neurosci. 17 (2003) 341-349
69. O'Keefe J., and Conway D.H. Hippocampal place units in the freely moving rat: why they fire where they fire. Exp. Brain Res. 31 (1978) 573-590
70. O'Keefe J., and Speakman A. Single unit activity in the rat hippocampus during a spatial memory task. Exp. Brain Res. 68 (1987) 1-27
71. Oorschot D.E. Are you using neuronal densities, synaptic densities or neurochemical densities as your definitive data? There is a better way to go. Prog. Neurobiol. 44 (1994) 233-247
72. Pandis C., Sotiriou E., Kouvaras E., Asprodini E., Papathedoropoulos C., and Angelatou F. Differential expression of NMDA and AMPA receptor subunits in rat dorsal and ventral hippocampus. Neuroscience 140 (2006) 163-175
73. Papatheodoropooulos C., and Kostopoulos G. Dorsal-ventral differentiation of short-term synaptic plasticity in rat CA1 hippocampal region. Neurosci. Lett. 286 (2000) 57-60
74. Papatheodoropooulos C., and Kostopoulos G. Decreased ability of rat temporal hippocampal CA1 region to produce long-term potentiation. Neurosci. Lett. 279 (2000) 177-180
75. Papatheodoropoulos C., Asprodini E., Nikita I., Koutsona C., and Kostopoulos G. Weaker synaptic inhibition in CA1 region of ventral compared to dorsal rat hippocampal slices. Brain Res. 948 (2002) 117-121
76. Papp E., Leinekugel X., Henze D.A., Lee J., and Buzsaki G. The apical shaft of CA1 pyramidal cells is under GABAergic interneuronal control. Neuroscience 102 (2001) 715-721
77. Piccini A., and Malinow R. Transient oxygen-glucose deprivation induces rapid morphological changes in rat hippocampal dendrites. Neuropharmacology 41 (2001) 724-729
78. Popken G.P., and Farel P.B. Reliability and validity of the physical disector method for estimating neuron number. J. Neurobiol. 31 (1996) 166-174
79. Quigg M., Bertram E.H., and Jackson T. Longitudinal distribution of hippocampal atrophy in mesial temporal lobe epilepsy. Epilepsy Res. 27 (1997) 101-110
80. Quirk G.J., Muller R.U., and Kubie J.L. The firing of hippocampal place cells in the dark reflects the rat's recent experience. J. Neurosci. 10 (1990) 2008-2017
81. Racine R., Rose P.A., and Burnham W.M. Afterdischarge thresholds and kindling rates in dorsal and ventral hippocampus and dentate gyrus. Can. J. Neurol. Sci. 4 (1977) 273-278
82. Rao B.S.S., Laxmi G.T.R., Meti B.L., and Raju T.R. Subicular lesions cause dendritic atrophy in CA1 and CA3 pyramidal neurons of the rat hippocampus. Neuroscience 102 (2001) 319-327
83. Robinson T.H., and Seiffert E.R. Afrotherian origins and interrelationships: new views and future prospects. Curr. Top. Dev. Biol. 63 (2004) 37-60
84. Rehkamper G. Vergleichende Architektonik des Neocortex der Insectivora. Z. f. Zool. Syst. Evolutforsch 19 (1981) 233-263
85. Roth L.R., and Leung L.S. Difference in LTP at basal and apical dendrites of CA1 pyramidal neurons in urethane-anesthetized rats. Brain Res. 694 (1995) 40-48
86. Row B.W., Goldbart A., Gozal E., and Gozal D. Spatial pre-training attenuates hippocampal impairments in rats exposed to intermittent hypoxia. Neurosci. Lett. 339 (2003) 67-71
87. Sajikumar S., and Frey J.U. Anisomycin inhibits the late maintenance of long-term depression in rat hippocampal slices in vitro. Neurosci. Lett. 338 (2003) 147-150
88. Salmanzadeh F., Fathollahi Y., Semnanian S., and Shafizadeh M. Dependence on morphine impairs the induction of long-term potentiation in the CA1 region of rat hippocampal slices. Brain Res. 965 (2003) 108-113
89. Sanabria E.R.G., Pereira M.F.S., Dolnikoff M.S., Andrade I.S., Ferreira A.T., Cavalheiro E.A., and Fernandes M.J.S. Deficit in hippocampal long-term potentiation in monosodium glutamate treated rats. Brain Res. Bull. 59 (2002) 47-51
90. Schwerdtfeger W.K., Danscher G., and Geiger H. Entorhinal and prepiriform cortices of the European Hedgehog. A histochemical and densitometric study based on a comparison between Timm's Sulphide Silver Method and the Selenium Method. Brain Res. 348 (1985) 69-76
91. Seress L. Morphological variability and developmental aspects of monkey and human granule cells: differences between the rodent and primate dentate gyrus. Epilepsy Res., Suppl. 7 (1992) 3-28
92. Shepherd G.M. Neurobiology. 2nd ed. (1988), Oxford University Press, New York
93. Shepherd G.M., and Koch C. Dendritic electrotonus and synaptic integration, in the synaptic organization of the brain (1990), Oxford University Press, New York
94. Shepherd G.M., Brayton R.K., Miller J.P., Segev I., Rinzel J., and Rall W. Signal enhancement in distal cortical dendrites by means of interactions between active dendritic spines. Proc. Natl. Acad. Sci. U. S. A. 82 (1985) 2192-2195
95. Sholl D.A. Dendritic organization of the neurons of the visual and motor cortices of the cat. J. Anat. 87 (1953) 387-406
96. Shults C.W., Johnston P., and Gage F.H. Comparison of substance K-like and substance P-like fibers and cells in the rat hippocampus. Brain Res. 426 (1987) 290-296
97. Simon R.P., Swan J.H., Griffiths T., and Meldrum B.S. Blockade of N-methyl-d-aspartate receptors may protect against ischemic damage in the brain. Science 226 (1984) 850-852
98. Sorra K.E., and Harris K.M. Stability in synapse number and size at 2 Hr after long-term potentiation in hippocampal area CA1. J. Neurosci. 18 (1998) 658-671
99. Sorra K.E., and Harris K.M. Overview on the structure, composition, function, development and plasticity of hippocampal dendritic spines. Hippocampus 10 (2000) 501-511
100. Sotiriou E., Papatheodoropoulos C., and Angelatou F. Differential expression of g-aminobutyric acid-A receptor subunits in rat dorsal and ventral hippocampus. J. Neurosci. Res. 82 (2005) 690-700
101. Spruston N., Jonas P., and Sakmann B. Dendritic glutamate receptor channels in rat hippocampal CA3 and CA1 pyramidal neurons. J. Physiol. 482 (1995) 325-352
102. Steele M.P., and Mauk M.D. Inhibitory control of LTP and LTD: stability of synapse strength. Am. Physiol. Soci. (1999) 1559-1566
103. Stephan H. Evolutionary trends in limbic structures. Neurosci. Biobehav. Rev. 7 (1983) 367-374
104. Stephan H., Baron G., and Frahm H. Comparative brain research in mammals. Insectivora, with a stereotaxic atlas of the hedgehog brain, Vol. 1 (1991), Springer-Verlag, New York
105. Stuart G., Spruston N., Sakmann B., and Hauser M. Action potential initation and backpropagation in neurons of the mammalian CNS. Trends Neurosci. 20 (1997) 125-131
106. Stuart G., Spruston N., and Hauser M. Dendrites (1999), Oxford University Press, New York
107. Thompson A.M., Gosnell B.A., and Wagner J.J. Enhancement of long-term potentiation in the rat hippocampus following cocaine exposure. Neuropharmacology 42 (2002) 1039-1042
108. Thompson K., Holm A.M., Scousboe A., Popper P., Micevych P., and Wasterlain C. Hippocampal stimulation produces neuronal death in the immature brain. Neuroscience 82 (1998) 337-348
109. 2+ in the rat hippocampal slice. J. Physiol. 478 (1994) 379-393
110. Van Groen T., and Wyss J.M. Extrinsic projections from area CA1 of. the rat hippocampus: olfactory, cortical, subcortical, and bilateral hippocampal formation projections. J. Comp. Neurol. 302 (1990) 515-528
111. West M.J., and Gundersen H.J.G. Unbiased stereological estimation of the number of neurons in the human hippocampus. J. Comp. Neurol. 296 (1990) 1-22
112. Witter M.P., Van Hoesen G.W., and Amaral D.G. Topographical organization of the entorhinal projection to the dentate gyrus of the monkey. J. Neurosci. 9 (1989) 216-228
113. IA receptor agonist ipsapirone on the local cerebral glucose utilization of the rat hippocampus. Brain Res. 436 (1987) 283-290
114. Wright J.W., and Harding J.W. The brain angiotensin system and extracellular matrix molecules in neural plasticity, learning and memory. Prog. Neurobiol. 72 (2004) 263-293
115. Yuste R., and Tank D.W. Dendritic integration in mammalian neurons, a century after Cajal. Neuron 16 (1996) 701-716
116. Zolman J. Biostatistics: Experimental Design and Statistical Inference (1993), Oxford University Press, New York