Reorganization of supramammillary–hippocampal pathways in the rat pilocarpine model of temporal lobe epilepsy: evidence for axon terminal sprouting

Brain Structure and Function

Volumn 220, Issue 4, 2015, Pages 2449-2468

  Soussi, Rabia ^a,b   Boulland, Jean Luc ^c   Bassot, Emilie ^a,b   Bras, Hélène ^b,d   Coulon, Patrice ^b,d   Chaudhry, Farrukh Abbas ^c   Storm Mathisen, Jon ^c   Ferhat, Lotfi ^b,e   Esclapez, Monique ^a,b  

^a AIX MARSEILLE UNIVERSITÉ   (France)

^b AIX MARSEILLE UNIVERSITY   (France)

^c UNIVERSITY OF OSLO   (Norway)

^d AIX MARSEILLE UNIVERSITÉ   (France)

^e Mediterranée University   (France)

Author keywords

Dentate gyrus; GAD; Hippocampus; Hypothalamus; SuM; VGAT; VGLUT2

Indexed keywords

DIAZEPAM; GLUTAMATE DECARBOXYLASE 65; LANTHANUM; MESSENGER RNA; NEURON SPECIFIC NUCLEAR PROTEIN; PILOCARPINE; VESICULAR GLUTAMATE TRANSPORTER 2; VESICULAR INHIBITORY AMINO ACID TRANSPORTER; BIOTIN; BIOTINYLATED DEXTRAN AMINE; DEXTRAN; ENOLASE; MUSCARINIC AGENT; SLC17A6 PROTEIN, RAT;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY LABELING; ARTICLE; BRAIN REGION; CONTROLLED STUDY; DENTATE GYRUS; EMOTION; EPILEPSY; GRANULE CELL; HYPOTHALAMUS NUCLEUS; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; LIMIT OF QUANTITATION; MALE; MEMORY; MESIAL TEMPORAL LOBE EPILEPSY; NERVE ENDING; NERVE SPROUTING; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RABIES VIRUS; RAT; SUPRAMAMMILLARY NUCLEUS; THETA RHYTHM; ANALOGS AND DERIVATIVES; ANIMAL; CHEMICALLY INDUCED; DISEASE MODEL; HIPPOCAMPUS; METABOLISM; NERVE TRACT; PATHOLOGY; PATHOPHYSIOLOGY; POSTERIOR HYPOTHALAMUS; TEMPORAL LOBE EPILEPSY; WISTAR RAT;

ANIMALIA; RATTUS;

ANIMALS; BIOTIN; DEXTRANS; DISEASE MODELS, ANIMAL; EPILEPSY, TEMPORAL LOBE; HIPPOCAMPUS; HYPOTHALAMUS, POSTERIOR; MALE; MUSCARINIC AGONISTS; NEURAL PATHWAYS; PHOSPHOPYRUVATE HYDRATASE; PILOCARPINE; PRESYNAPTIC TERMINALS; RABIES VIRUS; RATS; RATS, WISTAR; VESICULAR GLUTAMATE TRANSPORT PROTEIN 2;

EID: 84933183148     PISSN: 18632653     EISSN: 18632661     Source Type: Journal    
DOI: 10.1007/s00429-014-0800-2     Document Type: Article

References (91)

1. Abràmoff MD, Magelhaes PJ, Ram SJ (2004) Image processing with ImageJ. Biophotonics Int 11:36–42
2. Barroso-Chinea P, Castle M, Aymerich MS, Perez-Manso M, Erro E, Tunon T, Lanciego JL (2007) Expression of the mRNAs encoding for the vesicular glutamate transporters 1 and 2 in the rat thalamus. J Comp Neurol 501:703–715
3. Bettus G, Wendling F, Guye M, Valton L, Regis J, Chauvel P, Bartolomei F (2008) Enhanced EEG functional connectivity in mesial temporal lobe epilepsy. Epilepsy Res 81:58–68
4. Blümcke I, Suter B, Behle K, Kuhn R, Schramm J, Elger CE, Wiestler OD (2000) Loss of hilar mossy cells in Ammon’s horn sclerosis. Epilepsia 41:174–180
5. Boulland JL, Ferhat L, Tallak Solbu T, Ferrand N, Chaudhry FA, Storm-Mathisen J, Esclapez M (2007) Changes in vesicular transporters for gamma-aminobutyric acid and glutamate reveal vulnerability and reorganization of hippocampal neurons following pilocarpine-induced seizures. J Comp Neurol 503:466–485
6. Boulland JL, Jenstad M, Boekel AJ, Wouterlood FG, Edwards RH, Storm-Mathisen J, Chaudhry FA (2009) Vesicular glutamate and GABA transporters sort to distinct sets of vesicles in a population of presynaptic terminals. Cereb Cortex 19:241–248
7. Bras H, Gaytan SP, Portalier P, Zanella S, Pasaro R, Coulon P, Hilaire G (2008) Prenatal activation of 5-HT2A receptor induces expression of 5-HT1B receptor in phrenic motoneurons and alters the organization of their premotor network in newborn mice. Eur J Neurosci 28:1097–1107
8. Buckmaster PS, Zhang GF, Yamawaki R (2002) Axon sprouting in a model of temporal lobe epilepsy creates a predominantly excitatory feedback circuit. J Neurosci 22:6650–6658
9. Chai X, Münzner G, Zhao S, Tinnes S, Kowalski J, Häussler U, Young C, Haas CA, Frotscher M (2013) Epilepsy-induced motility of differentiated neurons. Cereb Cortex [Epub ahead of print]
10. Chaudhry FA, Reimer RJ, Bellocchio EE, Danbolt NC, Osen KK, Edwards RH, Storm-Mathisen J (1998) The vesicular GABA transporter, VGAT, localizes to synaptic vesicles in sets of glycinergic as well as GABAergic neurons. J Neurosci 18:9733–9750
11. Chauvière L, Rafrafi N, Thinus-Blanc C, Bartolomei F, Esclapez M, Bernard C (2009) Early deficits in spatial memory and theta rhythm in experimental temporal lobe epilepsy. J Neurosci 29:5402–5410
12. Colom LV, Castaneda MT, Reyna T, Hernandez S, Garrido-Sanabria E (2005) Characterization of medial septal glutamatergic neurons and their projection to the hippocampus. Synapse 58:151–164
13. Conrad LC, Leonard CM, Pfaff DW (1974) Connections of the median and dorsal raphe nuclei in the rat: an autoradiographic and degeneration study. J Comp Neurol 156:179–205
14. Cossart R, Dinocourt C, Hirsch JC, Merchan-Perez A, De Felipe J, Ben-Ari Y, Esclapez M, Bernard C (2001) Dendritic but not somatic GABAergic inhibition is decreased in experimental epilepsy. Nat Neurosci 4:52–62
15. Coulon P, Bras H, Vinay L (2011) Characterization of last-order premotor interneurons by transneuronal tracing with rabies virus in the neonatal mouse spinal cord. J Comp Neurol 519:3470–3487
16. Dashtipour K, Wong AM, Obenaus A, Spigelman I, Ribak CE (2003) Temporal profile of hilar basal dendrite formation on dentate granule cells after status epilepticus. Epilepsy Res 54:141–151
17. Deller T (1998) The anatomical organization of the rat fascia dentata: new aspects of laminar organization as revealed by anterograde tracing with Phaseolus vulgaris-Leucoagglutinin (PHAL). Anat Embryol (Berl) 197:89–103
18. Deller T, Martinez A, Nitsch R, Frotscher M (1996) A novel entorhinal projection to the rat dentate gyrus: direct innervation of proximal dendrites and cell bodies of granule cells and GABAergic neurons. J Neurosci 16:3322–3333
19. Dinocourt C, Petanjek Z, Freund TF, Ben-Ari Y, Esclapez M (2003) Loss of interneurons innervating pyramidal cell dendrites and axon initial segments in the CA1 region of the hippocampus following pilocarpine-induced seizures. J Comp Neurol 459:407–425
20. El-Hassar L, Milh M, Wendling F, Ferrand N, Esclapez M, Bernard C (2007) Cell domain-dependent changes in the glutamatergic and GABAergic drives during epileptogenesis in the rat CA1 region. J Physiol 578:193–211
21. Engel J (1996) Introduction to temporal lobe epilepsy. Epilepsy Res 26:141–150
22. Esclapez M, Houser CR (1999) Up-regulation of GAD65 and GAD67 in remaining hippocampal GABA neurons in a model of temporal lobe epilepsy. J Comp Neurol 412:488–505
23. Esclapez M, Tillakaratne NJ, Tobin AJ, Houser CR (1993) Comparative localization of mRNAs encoding two forms of glutamic acid decarboxylase with nonradioactive in situ hybridization methods. J Comp Neurol 331:339–362
24. Esclapez M, Tillakaratne NJ, Kaufman DL, Tobin AJ, Houser CR (1994) Comparative localization of two forms of glutamic acid decarboxylase and their mRNAs in rat brain supports the concept of functional differences between the forms. J Neurosci 14:1834–1855
25. Esclapez M, Hirsch JC, Khazipov R, Ben-Ari Y, Bernard C (1997) Operative GABAergic inhibition in hippocampal CA1 pyramidal neurons in experimental epilepsy. Proc Natl Acad Sci U S A 94:12151–12156
26. Esclapez M, Hirsch JC, Ben-Ari Y, Bernard C (1999) Newly formed excitatory pathways provide a substrate for hyperexcitability in experimental temporal lobe epilepsy. J Comp Neurol 408:449–460
27. Ferhat L, Esclapez M, Represa A, Fattoum A, Shirao T, Ben-Ari Y (2003) Increased levels of acidic calponin during dendritic spine plasticity after pilocarpine-induced seizures. Hippocampus 13:845–858
28. Fremeau RT Jr, Troyer MD, Pahner I, Nygaard GO, Tran CH, Reimer RJ, Bellocchio EE, Fortin D, Storm-Mathisen J, Edwards RH (2001) The expression of vesicular glutamate transporters defines two classes of excitatory synapse. Neuron 31:247–260
29. Fremeau RT Jr, Kam K, Qureshi T, Johnson J, Copenhagen DR, Storm-Mathisen J, Chaudhry FA, Nicoll RA, Edwards RH (2004) Vesicular glutamate transporters 1 and 2 target to functionally distinct synaptic release sites. Science 304:1815–1819
30. Freund TF, Antal M (1988) GABA-containing neurons in the septum control inhibitory interneurons in the hippocampus. Nature 336:170–173
31. Gaykema RP, Luiten PG, Nyakas C, Traber J (1990) Cortical projection patterns of the medial septum-diagonal band complex. J Comp Neurol 293:103–124
32. Gras C, Herzog E, Bellenchi GC, Bernard V, Ravassard P, Pohl M, Gasnier B, Giros B, El Mestikawy S (2002) A third vesicular glutamate transporter expressed by cholinergic and serotoninergic neurons. J Neurosci 22:5442–5451
33. Gritti I, Henny P, Galloni F, Mainville L, Mariotti M, Jones BE (2006) Stereological estimates of the basal forebrain cell population in the rat, including neurons containing choline acetyltransferase, glutamic acid decarboxylase or phosphate-activated glutaminase and colocalizing vesicular glutamate transporters. Neuroscience 143:1051–1064
34. Haas CA, Dudeck O, Kirsch M, Huszka C, Kann G, Pollak S, Zentner J, Frotscher M (2002) Role for reelin in the development of granule cell dispersion in temporal lobe epilepsy. J Neurosci 22:5797–5802
35. Haglund L, Swanson LW, Köhler C (1984) The projection of the supramammillary nucleus to the hippocampal formation: an immunohistochemical and anterograde transport study with the lectin PHA-L in the rat. J Comp Neurol 229:171–185
36. Halasy K, Hajszan T, Kovacs EG, Lam TT, Leranth C (2004) Distribution and origin of vesicular glutamate transporter 2-immunoreactive fibers in the rat hippocampus. Hippocampus 14:908–918
37. Herzog E, Bellenchi GC, Gras C, Bernard V, Ravassard P, Bedet C, Gasnier B, Giros B, El Mestikawy S (2001) The existence of a second vesicular glutamate transporter specifies subpopulations of glutamatergic neurons. J Neurosci 21:RC181
38. Herzog E, Gilchrist J, Gras C, Muzerelle A, Ravassard P, Giros B, Gaspar P, El Mestikawy S (2004) Localization of VGLUT3, the vesicular glutamate transporter type 3, in the rat brain. Neuroscience 123:983–1002
39. Herzog E, Takamori S, Jahn R, Brose N, Wojcik SM (2006) Synaptic and vesicular co-localization of the glutamate transporters VGLUT1 and VGLUT2 in the mouse hippocampus. J Neurochem 99:1011–1018
40. Hoover WB, Vertes RP (2012) Collateral projections from nucleus reuniens of thalamus to hippocampus and medial prefrontal cortex in the rat: a single and double retrograde fluorescent labeling study. Brain Struct Funct 217:191–209
41. Houser CR (1990) Granule cell dispersion in the dentate gyrus of humans with temporal lobe epilepsy. Brain Res 535:195–204
42. Houser CR, Esclapez M (1996) Vulnerability and plasticity of the GABA system in the pilocarpine model of spontaneous recurrent seizures. Epilepsy Res 26:207–218
43. Jiao Y, Nadler JV (2007) Stereological analysis of GluR2-immunoreactive hilar neurons in the pilocarpine model of temporal lobe epilepsy: correlation of cell loss with mossy fiber sprouting. Exp Neurol 205:569–582
44. Kahane P, Bartolomei F (2010) Temporal lobe epilepsy and hippocampal sclerosis: lessons from depth EEG recordings. Epilepsia 51:59–62
45. Kaneko T, Fujiyama F, Hioki H (2002) Immunohistochemical localization of candidates for vesicular glutamate transporters in the rat brain. J Comp Neurol 444:39–62
46. Kienzler F, Norwood BA, Sloviter RS (2009) Hippocampal injury, atrophy, synaptic reorganization, and epileptogenesis after perforant pathway stimulation-induced status epilepticus in the mouse. J Comp Neurol 515:181–196
47. Kirk IJ, McNaughton N (1991) Supramammillary cell firing and hippocampal rhythmical slow activity. Neuroreport 2:723–725
48. Kirk IJ, McNaughton N (1993) Mapping the differential effects of procaine on frequency and amplitude of reticularly elicited hippocampal rhythmical slow activity. Hippocampus 3:517–525
49. Kobayashi M, Buckmaster PS (2003) Reduced inhibition of dentate granule cells in a model of temporal lobe epilepsy. J Neurosci 23:2440–2452
50. Kocsis B, Kaminski M (2006) Dynamic changes in the direction of the theta rhythmic drive between supramammillary nucleus and the septohippocampal system. Hippocampus 16:531–540
51. Kocsis B, Vertes RP (1994) Characterization of neurons of the supramammillary nucleus and mammillary body that discharge rhythmically with the hippocampal theta rhythm in the rat. J Neurosci 14:7040–7052
52. Köhler C, Haglund L, Swanson LW (1984) A diffuse alpha MSH-immunoreactive projection to the hippocampus and spinal cord from individual neurons in the lateral hypothalamic area and zona incerta. J Comp Neurol 223:501–514
53. Köhler C, Swanson LW, Haglund L, Wu JY (1985) The cytoarchitecture, histochemistry and projections of the tuberomammillary nucleus in the rat. Neuroscience 16:85–110
54. Lanteaume L, Bartolomei F, Bastien-Toniazzo M (2009) How do cognition, emotion, and epileptogenesis meet? A study of emotional cognitive bias in temporal lobe epilepsy. Epilepsy Behav 15:218–224
55. Lehmann TN, Gabriel S, Eilers A, Njunting M, Kovacs R, Schulze K, Lanksch WR, Heinemann U (2001) Fluorescent tracer in pilocarpine-treated rats shows widespread aberrant hippocampal neuronal connectivity. Eur J Neurosci 14:83–95
56. Lowenstein DH, Thomas MJ, Smith DH, McIntosh TK (1992) Selective vulnerability of dentate hilar neurons following traumatic brain injury: a potential mechanistic link between head trauma and disorders of the hippocampus. J Neurosci 12:4846–4853
57. Maglóczky Z, Acsady L, Freund TF (1994) Principal cells are the postsynaptic targets of supramammillary afferents in the hippocampus of the rat. Hippocampus 4:322–334
58. Maglóczky Z, Wittner L, Borhegyi Z, Halasz P, Vajda J, Czirjak S, Freund TF (2000) Changes in the distribution and connectivity of interneurons in the epileptic human dentate gyrus. Neuroscience 96:7–25
59. Marcelin B, Chauviere L, Becker A, Migliore M, Esclapez M, Bernard C (2009) h channel-dependent deficit of theta oscillation resonance and phase shift in temporal lobe epilepsy. Neurobiol Dis 33:436–447
60. McIntire SL, Reimer RJ, Schuske K, Edwards RH, Jorgensen EM (1997) Identification and characterization of the vesicular GABA transporter. Nature 389:870–876
61. Mello LE, Cavalheiro EA, Tan AM, Kupfer WR, Pretorius JK, Babb TL, Finch DM (1993) Circuit mechanisms of seizures in the pilocarpine model of chronic epilepsy: cell loss and mossy fiber sprouting. Epilepsia 34:985–995
62. Nyakas C, Luiten PG, Spencer DG, Traber J (1987) Detailed projection patterns of septal and diagonal band efferents to the hippocampus in the rat with emphasis on innervation of CA1 and dentate gyrus. Brain Res Bull 18:533–545
63. Obenaus A, Esclapez M, Houser CR (1993) Loss of glutamate decarboxylase mRNA-containing neurons in the rat dentate gyrus following pilocarpine-induced seizures. J Neurosci 13:4470–4485
64. Okazaki MM, Nadler JV (2001) Glutamate receptor involvement in dentate granule cell epileptiform activity evoked by mossy fiber stimulation. Brain Res 915:58–69
65. Okazaki MM, Evenson DA, Nadler JV (1995) Hippocampal mossy fiber sprouting and synapse formation after status epilepticus in rats: visualization after retrograde transport of biocytin. J Comp Neurol 352:515–534
66. Pan WX, McNaughton N (2002) The role of the medial supramammillary nucleus in the control of hippocampal theta activity and behaviour in rats. Eur J Neurosci 16:1797–1809
67. Pan WX, McNaughton N (2004) The supramammillary area: its organization, functions and relationship to the hippocampus. Prog Neurobiol 74:127–166
68. Pasquier DA, Reinoso-Suarez F (1976) Direct projections from hypothalamus to hippocampus in the rat demonstrated by retrograde transport of horseradish peroxidase. Brain Res 108:165–169
69. Peng Z, Zhang N, Wei W, Huang CS, Cetina Y, Otis TS, Houser CR (2013) A reorganized GABAergic circuit in a model of epilepsy: evidence from optogenetic labeling and stimulation of somatostatin interneurons. J Neurosci 33:14392–14405
70. Raux H, Iseni F, Lafay F, Blondel D (1997) Mapping of monoclonal antibody epitopes of the rabies virus P protein. J Gen Virol 78(Pt 1):119–124
71. Ribak CE, Shapiro LA, Yan XX, Dashtipour K, Nadler JV, Obenaus A, Spigelman I, Buckmaster PS (2012) Seizure-induced formation of basal dendrites on granule cells of the rodent dentate gyrus. In: Noebels JL, Avoli M, Rogawski MA, Olsen RW, Delgado-Escueta AV (eds) Jasper’s basic mechanisms of the epilepsies, 4th edn
72. Richmond MA, Yee BK, Pouzet B, Veenman L, Rawlins JN, Feldon J, Bannerman DM (1999) Dissociating context and space within the hippocampus: effects of complete, dorsal, and ventral excitotoxic hippocampal lesions on conditioned freezing and spatial learning. Behav Neurosci 113:1189–1203
73. Saji M, Kobayashi S, Ohno K, Sekino Y (2000) Interruption of supramammillohippocampal afferents prevents the genesis and spread of limbic seizures in the hippocampus via a disinhibition mechanism. Neuroscience 97:437–445
74. Salin P, Castle M, Kachidian P, Barroso-Chinea P, Lopez IP, Rico AJ, Kerkerian-Le Goff L, Coulon P, Lanciego JL (2008) High-resolution neuroanatomical tract-tracing for the analysis of striatal microcircuits. Brain Res 1221:49–58
75. Santin LJ, Aguirre JA, Rubio S, Begega A, Miranda R, Arias JL (2003) c-Fos expression in supramammillary and medial mammillary nuclei following spatial reference and working memory tasks. Physiol Behav 78:733–739
76. Sbai O, Khrestchatisky M, Esclapez M, Ferhat L (2012) Drebrin A expression is altered after pilocarpine-induced seizures: time course of changes is consistent for a role in the integrity and stability of dendritic spines of hippocampal granule cells. Hippocampus 22:477–493
77. Shahidi S, Motamedi F, Bakeshloo SA, Taleghani BK (2004) The effect of reversible inactivation of the supramammillary nucleus on passive avoidance learning in rats. Behav Brain Res 152:81–87
78. Skyers PS, Einheber S, Pierce JP, Milner TA (2003) Increased mu-opioid receptor labeling is found on inner molecular layer terminals of the dentate gyrus following seizures. Exp Neurol 179:200–2009
79. Sloviter RS (1987) Decreased hippocampal inhibition and a selective loss of interneurons in experimental epilepsy. Science 235:73–76
80. Sloviter RS (1991) Permanently altered hippocampal structure, excitability, and inhibition after experimental status epilepticus in the rat: the “dormant basket cell” hypothesis and its possible relevance to temporal lobe epilepsy. Hippocampus 1:41–66
81. Sloviter RS, Zappone CA, Harvey BD, Bumanglag AV, Bender RA, Frotscher M (2003) “Dormant basket cell” hypothesis revisited: relative vulnerabilities of dentate gyrus mossy cells and inhibitory interneurons after hippocampal status epilepticus in the rat. J Comp Neurol 459:44–76
82. Soussi R, Zhang N, Tahtakran S, Houser CR, Esclapez M (2010) Heterogeneity of the supramammillary-hippocampal pathways: evidence for a unique GABAergic neurotransmitter phenotype and regional differences. Eur J Neurosci 32:771–785
83. Ugolini G (2010) Advances in viral transneuronal tracing. J Neurosci Methods 194:2–20
84. Vertes RP (1992) PHA-L analysis of projections from the supramammillary nucleus in the rat. J Comp Neurol 326:595–622
85. Vertes RP, Kocsis B (1997) Brainstem-diencephalo-septohippocampal systems controlling the theta rhythm of the hippocampus. Neuroscience 81:893–926
86. Vertes RP, McKenna JT (2000) Collateral projections from the supramammillary nucleus to the medial septum and hippocampus. Synapse 38:281–293
87. Vertes RP, Fortin WJ, Crane AM (1999) Projections of the median raphe nucleus in the rat. J Comp Neurol 407:555–582
88. Wieser HG (2004) ILAE Commission Report. Mesial temporal lobe epilepsy with hippocampal sclerosis. Epilepsia 45:695–714
89. Williams PA, White AM, Clark S, Ferraro DJ, Swiercz W, Staley KJ, Dudek FE (2009) Development of spontaneous recurrent seizures after kainate-induced status epilepticus. J Neurosci 29:2103–2112
90. Wouterlood FG, Saldana E, Witter MP (1990) Projection from the nucleus reuniens thalami to the hippocampal region: light and electron microscopic tracing study in the rat with the anterograde tracer Phaseolus vulgaris-leucoagglutinin. J Comp Neurol 296:179–203
91. Zappone CA, Sloviter RS (2004) Translamellar disinhibition in the rat hippocampal dentate gyrus after seizure-induced degeneration of vulnerable hilar neurons. J Neurosci 24:853–864