Identification of dorsal–ventral hippocampal differentiation in neonatal rats

Brain Structure and Function

Volumn 220, Issue 5, 2015, Pages 2873-2893

  O’Reilly, Kally C ^a,b   Flatberg, Arnar ^a   Islam, Sobia ^a   Olsen, Lene C ^a   Kruge, Ingvild Ulsaker ^a   Witter, Menno P ^a  

^a NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

^b NEW YORK UNIVERSITY   (United States)

Author keywords

Development; Dorsal ventral hippocampus; Entorhinal hippocampal connectivity; Hippocampal transcription

Indexed keywords

ALCOHOLISM; ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY DISORDER; ARTICLE; CONTROLLED STUDY; DENTATE GYRUS; DEVELOPMENTAL STAGE; DORSAL VENTRAL HIPPOCAMPUS; ENTORHINAL CORTEX; GENE EXPRESSION; GENE EXPRESSION PROFILING; HIPPOCAMPAL TISSUE; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MEDIAL ENTORHINAL CORTEX; MENTAL DISEASE; MICROTOME; MORPHOMETRICS; NEWBORN; NONHUMAN; PHASEOLUS VULGARIS; PRINCIPAL COMPONENT ANALYSIS; PRIORITY JOURNAL; RAT; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION; SCHIZOPHRENIA; STEREOTAXIC SURGERY; UPREGULATION; VENTRAL HIPPOCAMPUS; ANIMAL; BRAIN MAPPING; DISEASE MODEL; FEMALE; LONG EVANS RAT; MALE; METABOLISM; PATHOLOGY; PHYSIOLOGY; PROCEDURES;

ANIMALS; ANIMALS, NEWBORN; BRAIN MAPPING; DISEASE MODELS, ANIMAL; ENTORHINAL CORTEX; FEMALE; GENE EXPRESSION; HIPPOCAMPUS; MALE; MENTAL DISORDERS; RATS, LONG-EVANS;

EID: 84940584157     PISSN: 18632653     EISSN: 18632661     Source Type: Journal    
DOI: 10.1007/s00429-014-0831-8     Document Type: Article

References (69)

1. Abdulla FA, Bradbury E, Calaminici MR, Lippiello PM, Wonnacott S, Gray JA, Sinden JD (1996) Relationship between up-regulation of nicotine binding sites in rat brain and delayed cognitive enhancement observed after chronic or acute nicotinic receptor stimulation. Psychopharmacology 124(4):323–331
2. Alberi L, Liu S, Wang Y, Badie R, Smith-Hicks C, Wu J, Pierfelice TJ, Abazyan B, Mattson MP, Kuhl D, Pletnikov M, Worley PF, Gaiano N (2011) Activity-induced Notch signaling in neurons requires Arc/Arg3.1 and is essential for synaptic plasticity in hippocampal networks. Neuron 69(3):437–444. doi:10.1016/j.neuron.2011.01.004
3. Andersen CL, Jensen JL, Orntoft TF (2004) Normalization of real-time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res 64(15):5245–5250. doi:10.1158/0008-5472.CAN-04-0496
4. Ansorge MS, Hen R, Gingrich JA (2007) Neurodevelopmental origins of depressive disorders. Curr Opin Pharmacol 7(1):8–17. doi:10.1016/j.coph.2006.11.006
5. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G (2000) Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 25(1):25–29. doi:10.1038/75556
6. Bachevalier J, Beauregard M (1993) Maturation of medial temporal lobe memory functions in rodents, monkeys, and humans. Hippocampus 3 Spec No:191–201
7. Bannerman DM, Yee BK, Good MA, Heupel MJ, Iversen SD, Rawlins JN (1999) Double dissociation of function within the hippocampus: a comparison of dorsal, ventral, and complete hippocampal cytotoxic lesions. Behav Neurosci 113(6):1170–1188
8. Bannerman DM, Grubb M, Deacon RM, Yee BK, Feldon J, Rawlins JN (2003) Ventral hippocampal lesions affect anxiety but not spatial learning. Behav Brain Res 139(1–2):197–213
9. Bannerman DM, Rawlins JN, McHugh SB, Deacon RM, Yee BK, Bast T, Zhang WN, Pothuizen HH, Feldon J (2004) Regional dissociations within the hippocampus—memory and anxiety. Neurosci Biobehav Rev 28(3):273–283. doi:10.1016/j.neubiorev.2004.03.004
10. Bayer SA (1980) Development of the hippocampal region in the rat. I. Neurogenesis examined with 3H-thymidine autoradiography. J Comp Neurol 190(1):87–114. doi:10.1002/cne.901900107
11. Brooks JM, Sarter M, Bruno JP (2011) Transient inactivation of the neonatal ventral hippocampus permanently disrupts the mesolimbic regulation of prefrontal cholinergic transmission: implications for schizophrenia. Neuropsychopharmacology 36(12):2477–2487. doi:10.1038/npp.2011.136
12. Chen DY, Stern SA, Garcia-Osta A, Saunier-Rebori B, Pollonini G, Bambah-Mukku D, Blitzer RD, Alberini CM (2011) A critical role for IGF-II in memory consolidation and enhancement. Nature 469(7331):491–497. doi:10.1038/nature09667
13. Christensen T, Bisgaard CF, Nielsen HB, Wiborg O (2010) Transcriptome differentiation along the dorso-ventral axis in laser-captured microdissected rat hippocampal granular cell layer. Neuroscience 170(3):731–741. doi:10.1016/j.neuroscience.2010.07.016
14. Costa RM, Honjo T, Silva AJ (2003) Learning and memory deficits in Notch mutant mice. Curr Biol 13(15):1348–1354
15. Czerniawski J, Yoon T, Otto T (2009) Dissociating space and trace in dorsal and ventral hippocampus. Hippocampus 19(1):20–32. doi:10.1002/hipo.20469
16. Deng JB, Yu DM, Wu P, Li MS (2007) The tracing study of developing entorhino-hippocampal pathway. Int J Dev Neurosci 25(4):251–258. doi:10.1016/j.ijdevneu.2007.03.002
17. Dolorfo CL, Amaral DG (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(1):25–48. doi:10.1002/(SICI)1096-9861
18. Dong HW, Swanson LW, Chen L, Fanselow MS, Toga AW (2009) Genomic-anatomic evidence for distinct functional domains in hippocampal field CA1. Proc Natl Acad Sci USA 106(28):11794–11799. doi:10.1073/pnas.0812608106
19. Fanselow MS, Dong HW (2010) Are the dorsal and ventral hippocampus functionally distinct structures? Neuron 65(1):7–19. doi:10.1016/j.neuron.2009.11.031
20. Forster E, Zhao S, Frotscher M (2006) Laminating the hippocampus. Nat Rev Neurosci 7(4):259–267. doi:10.1038/nrn1882
21. Freedman R, Goldowitz D (2010) Studies on the hippocampal formation: from basic development to clinical applications: studies on schizophrenia. Prog Neurobiol 90(2):263–275. doi:10.1016/j.pneurobio.2009.10.008
22. Insausti R, Amaral DG (2004) Hippocampal formation. In: Paxinos G, Mai JK (eds) The human nervous system. Elsevier Academic Press, San Diego, pp 872–915
23. Jacobson S (1963) Sequence of myelinization in the brain of the albino rat. A. Cerebral cortex, thalamus and related structures. J Comp Neurol 121:5–29
24. Jinno S, Kosaka T (2006) Cellular architecture of the mouse hippocampus: a quantitative aspect of chemically defined GABAergic neurons with stereology. Neurosci Res 56(3):229–245. doi:10.1016/j.neures.2006.07.007
25. Jinno S, Kosaka T (2010) Stereological estimation of numerical densities of glutamatergic principal neurons in the mouse hippocampus. Hippocampus 20(7):829–840. doi:10.1002/hipo.20685
26. Kenney JW, Raybuck JD, Gould TJ (2012) Nicotinic receptors in the dorsal and ventral hippocampus differentially modulate contextual fear conditioning. Hippocampus 22(8):1681–1690. doi:10.1002/hipo.22003
27. Kjelstrup KB, Solstad T, Brun VH, Hafting T, Leutgeb S, Witter MP, Moser EI, Moser MB (2008) Finite scale of spatial representation in the hippocampus. Science 321(5885):140–143. doi:10.1126/science.1157086
28. Lagali PS, Corcoran CP, Picketts DJ (2010) Hippocampus development and function: role of epigenetic factors and implications for cognitive disease. Clin Genet 78(4):321–333. doi:10.1111/j.1399-0004.2010.01503.x
29. Law AJ, Pei Q, Walker M, Gordon-Andrews H, Weickert CS, Feldon J, Pryce CR, Harrison PJ (2009) Early parental deprivation in the marmoset monkey produces long-term changes in hippocampal expression of genes involved in synaptic plasticity and implicated in mood disorder. Neuropsychopharmacology 34(6):1381–1394. doi:10.1038/npp.2008.106
30. Leonardo ED, Richardson-Jones JW, Sibille E, Kottman A, Hen R (2006) Molecular heterogeneity along the dorsal–ventral axis of the murine hippocampal CA1 field: a microarray analysis of gene expression. Neuroscience 137(1):177–186. doi:10.1016/j.neuroscience.2005.08.082
31. Lillrank SM, Lipska BK, Weinberger DR (1995) Neurodevelopmental animal models of schizophrenia. Clin Neurosci 3(2):98–104
32. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25(4):402–408. doi:10.1006/meth.2001.1262
33. Louvi A, Artavanis-Tsakonas S (2006) Notch signalling in vertebrate neural development. Nat Rev Neurosci 7(2):93–102. doi:10.1038/nrn1847
34. Meier S, Brauer AU, Heimrich B, Nitsch R, Savaskan NE (2004) Myelination in the hippocampus during development and following lesion. Cell Mol Life Sci 61(9):1082–1094. doi:10.1007/s00018-004-3469-5
35. Meyer F, Peterschmitt Y, Louilot A (2009) Postnatal functional inactivation of the entorhinal cortex or ventral subiculum has different consequences for latent inhibition-related striatal dopaminergic responses in adult rats. Eur J Neurosci 29(10):2035–2048. doi:10.1111/j.1460-9568.2009.06755.x
36. Moser MB, Moser EI (1998) Functional differentiation in the hippocampus. Hippocampus 8(6):608–619. doi:10.1002/(SICI)1098-1063
37. Moser E, Moser MB, Andersen P (1993) Spatial learning impairment parallels the magnitude of dorsal hippocampal lesions, but is hardly present following ventral lesions. J Neurosci 13(9):3916–3925
38. Moser MB, Moser EI, Forrest E, Andersen P, Morris RG (1995) Spatial learning with a minislab in the dorsal hippocampus. Proc Natl Acad Sci USA 92(21):9697–9701
39. Narr KL, Thompson PM, Szeszko P, Robinson D, Jang S, Woods RP, Kim S, Hayashi KM, Asunction D, Toga AW, Bilder RM (2004) Regional specificity of hippocampal volume reductions in first-episode schizophrenia. Neuroimage 21(4):1563–1575. doi:10.1016/j.neuroimage.2003.11.011
40. O’Reilly KC, Gulden Dahl A, Ulsaker Kruge I, Witter MP (2013) Subicular–parahippocampal projections revisited: development of a complex topography in the rat. J Comp Neurol 521(18):4284–4299. doi:10.1002/cne.23417
41. Patel J, Fujisawa S, Berenyi A, Royer S, Buzsaki G (2012) Traveling theta waves along the entire septotemporal axis of the hippocampus. Neuron 75(3):410–417. doi:10.1016/j.neuron.2012.07.015
42. Paxinos G, Watson C (2007) The rat brain in stereotaxic coordinates, 6th edn. Elsevier Inc., London
43. Pokorny J, Yamamoto T (1981) Postnatal ontogenesis of hippocampal CA1 area in rats. I. Development of dendritic arborisation in pyramidal neurons. Brain Res Bull 7(2):113–120
44. Posener JA, Wang L, Price JL, Gado MH, Province MA, Miller MI, Babb CM, Csernansky JG (2003) High-dimensional mapping of the hippocampus in depression. Am J Psychiatry 160(1):83–89
45. Royer S, Sirota A, Patel J, Buzsaki G (2010) Distinct representations and theta dynamics in dorsal and ventral hippocampus. J Neurosci 30(5):1777–1787. doi:10.1523/JNEUROSCI.4681-09.2010
46. Rudy JW, Morledge P (1994) Ontogeny of contextual fear conditioning in rats: implications for consolidation, infantile amnesia, and hippocampal system function. Behav Neurosci 108(2):227–234
47. Sansom SN, Livesey FJ (2009) Gradients in the brain: the control of the development of form and function in the cerebral cortex. Cold Spring Harb Perspect Biol 1(2):a002519. doi:10.1101/cshperspect.a002519
48. Schenk F (1985) Development of place navigation in rats from weaning to puberty. Behav Neural Biol 43(1):69–85
49. Schlessinger AR, Cowan WM, Swanson LW (1978) The time of origin of neurons in Ammon’s horn and the associated retrohippocampal fields. Anat Embryol (Berl) 154(2):153–173
50. Segal M, Richter-Levin G, Maggio N (2010) Stress-induced dynamic routing of hippocampal connectivity: a hypothesis. Hippocampus 20(12):1332–1338. doi:10.1002/hipo.20751
51. Small SA, Schobel SA, Buxton RB, Witter MP, Barnes CA (2011) A pathophysiological framework of hippocampal dysfunction in ageing and disease. Nat Rev Neurosci 12(10):585–601. doi:10.1038/nrn3085
52. Smith GN, Lang DJ, Kopala LC, Lapointe JS, Falkai P, Honer WG (2003) Developmental abnormalities of the hippocampus in first-episode schizophrenia. Biol Psychiatry 53(7):555–561
53. Smyth GK (2004) Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3:Article3. doi:10.2202/1544-6115.1027
54. Steffenach HA, Witter MP, Moser MB, Moser EI (2005) Spatial memory in the rat requires the dorsolateral band of the entorhinal cortex. Neuron 45(2):301–313
55. Tamamaki N (1999) Development of afferent fiber lamination in the infrapyramidal blade of the rat dentate gyrus. J Comp Neurol 411(2):257–266. doi:10.1002/(SICI)1096-9861
56. Thompson CL, Pathak SD, Jeromin A, Ng LL, MacPherson CR, Mortrud MT, Cusick A, Riley ZL, Sunkin SM, Bernard A, Puchalski RB, Gage FH, Jones AR, Bajic VB, Hawrylycz MJ, Lein ES (2008) Genomic anatomy of the hippocampus. Neuron 60(6):1010–1021. doi:10.1016/j.neuron.2008.12.008
57. Tseng KY, Chambers RA, Lipska BK (2009) The neonatal ventral hippocampal lesion as a heuristic neurodevelopmental model of schizophrenia. Behav Brain Res 204(2):295–305. doi:10.1016/j.bbr.2008.11.039
58. van Groen T, Miettinen P, Kadish I (2003) The entorhinal cortex of the mouse: organization of the projection to the hippocampal formation. Hippocampus 13(1):133–149. doi:10.1002/hipo.10037
59. van Strien NM, Cappaert NL, Witter MP (2009) The anatomy of memory: an interactive overview of the parahippocampal–hippocampal network. Nat Rev Neurosci 10(4):272–282. doi:10.1038/nrn2614
60. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3(7):RESEARCH0034
61. Wang Y, Chan SL, Miele L, Yao PJ, Mackes J, Ingram DK, Mattson MP, Furukawa K (2004) Involvement of Notch signaling in hippocampal synaptic plasticity. Proc Natl Acad Sci USA 101(25):9458–9462. doi:10.1073/pnas.0308126101
62. Witter MP (1989) Connectivity of the rat hippocampus. In: Chan-Palay V, Köhler C (eds) The Hippocampus—new vistas, neurology and neurobiology, vol 52. Alan R. Liss Inc., New York, pp 53–69
63. Witter MP (2007a) Intrinsic and extrinsic wiring of CA3: indications for connectional heterogeneity. Learn Mem 14(11):705–713. doi:10.1101/lm.725207
64. Witter MP (2007b) The perforant path: projections from the entorhinal cortex to the dentate gyrus. Prog Brain Res 163:43–61. doi:10.1016/S0079-6123(07)63003-9
65. Witter MP, Amaral DG (2004) The hippocampal region. In: Paxinos G (ed) The rat nervous system, 3rd edn. Elsevier Academic Press, San Diego, pp 637–703
66. Witter MP, Groenewegen HJ (1984) Laminar origin and septotemporal distribution of entorhinal and perirhinal projections to the hippocampus in the cat. J Comp Neurol 224(3):371–385. doi:10.1002/cne.902240305
67. Witter MP, Van Hoesen GW, Amaral DG (1989) Topographical organization of the entorhinal projection to the dentate gyrus of the monkey. J Neurosci 9(1):216–228
68. Witter MP, Naber PA, van Haeften T, Machielsen WC, Rombouts SA, Barkhof F, Scheltens P, Lopes da Silva FH (2000a) Cortico-hippocampal communication by way of parallel parahippocampal-subicular pathways. Hippocampus 10(4):398–410. doi:10.1002/1098-1063
69. Witter MP, Wouterlood FG, Naber PA, Van Haeften T (2000b) Anatomical organization of the parahippocampal–hippocampal network. Ann N Y Acad Sci 911:1–24