Translamellar Disinhibition in the Rat Hippocampal Dentate Gyrus after Seizure-Induced Degeneration of Vulnerable Hilar Neurons

Journal of Neuroscience

Volumn 24, Issue 4, 2004, Pages 853-864

  Zappone, Colin A ^a   Sloviter, Robert S ^a  

^a UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

Author keywords

c Fos; Epilepsy; Hippocampus; Inhibitory interneurons; Lamellar hypothesis; Lateral inhibition

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR BLOCKING AGENT; BICUCULLINE METHIODIDE; FLUOROGOLD; KAINIC ACID; PROTEIN C FOS; SOMATOSTATIN; URETHAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DENTATE GYRUS; DIFFUSION; ELECTRODE; EPILEPSY; EPILEPTIC STATE; EVOKED RESPONSE; GENE EXPRESSION; GRANULE CELL; HIPPOCAMPUS; HYPOTHESIS; INTERNEURON; MALE; MOSSY FIBER; NERVE CELL DEGENERATION; NERVE CELL EXCITABILITY; NERVE CELL INHIBITION; NERVE PROJECTION; NONHUMAN; ONCOGENE C FOS; PRIORITY JOURNAL; RAT; RETROGRADE NERVE FIBER TRANSPORT; SEIZURE;

ANIMALS; AXONAL TRANSPORT; CELL SURVIVAL; DENTATE GYRUS; DIFFUSION; ELECTRIC STIMULATION; FLUORESCENT DYES; GABA ANTAGONISTS; HIPPOCAMPUS; KAINIC ACID; MALE; NERVE DEGENERATION; NEURAL INHIBITION; NEURONS; PERFORANT PATHWAY; PROTO-ONCOGENE PROTEINS C-FOS; RATS; RATS, SPRAGUE-DAWLEY; SEIZURES; STILBAMIDINES;

EID: 0742305191     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1619-03.2004     Document Type: Article

References (52)

1. Amaral DG (1978) A Golgi study of cell types in the hilar region of the hippocampus in the rat. J Comp Neurol 182:851-914.
2. Amaral DG, Witter MP (1989) The three-dimensional organization of the hippocampal formation: a review of anatomical data. Neuroscience 31:571-591.
3. Andersen P, Holmqvist B, Voorhoeve PE (1966) Entorhinal activation of dentate granule cells. Acta Physiol Scand 66:448-460.
4. Andersen P, Bliss TVP, Skrede KK (1971) Lamellar organization of hippocampal excitatory pathways. Exp Brain Res 13:222-238.
5. Andersen P, Soleng AF, Raastad M (2000) The hippocampal lamella hypothesis revisited. Brain Res 886:165-171.
6. Bakst I, Avendano C, Morrison JH, Amaral DG (1986) An experimental analysis of the origins of somatostatin-like immunoreactivity in the dentate gyrus of the rat. J Neurosci 6:1452-1462.
7. Bekenstein JW, Lothman EW (1991) Electrophysiological characterization of associational pathway terminating on dentate gyrus granule cells in the rat. Hippocampus 1:399-404.
8. 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 [Suppl 6]:S174-S180.
9. Brooks-Kayal AR, Shumate MD, Jin H, Rikhter TY, Coulter DA (1998) Selective changes in single cell GABA(A) receptor subunit expression and function in temporal lobe epilepsy. Nat Med 4:1166-1172.
10. Buckmaster PS, Dudek FE (1997) Network properties of the dentate gyrus in epileptic rats with hilar neuron loss and granule cell axon reorganization. J Neurophysiol 77:2685-2696.
11. Buckmaster PS, Dudek FE (1999) In vivo intracellular analysis of granule cell axon reorganization in epileptic rats. J Neurophysiol 81:712-721.
12. Buckmaster PS, Jongen-Rêlo AL (1999) Highly specific neuron loss preserves lateral inhibitory circuits in the dentate gyrus of kainate-induced epileptic rats. J Neurosci 19:9519-9529.
13. Buckmaster PS, Schwartzkroin PA (1994) Hippocampal mossy cell function: a speculative view. Hippocampus 4:393-402.
14. Buckmaster PS, Schwartzkroin PA (1995) Interneurons and inhibition in the dentate gyrus of the rat in vivo. J Neurosci 15:774-789.
15. Buckmaster PS, Wenzel HJ, Kunkel DD, Schwartzkroin PA (1996) Axon arbors and synaptic connections of hippocampal mossy cells in the rat in vivo. J Comp Neurol 366:271-292.
16. Bureau I, Bischoff S, Heinemann SF, Mulle C (1999) Kainate receptor-mediated responses in the CA1 field of wild-type and GluR6-deficient mice. J Neurosci 19:653-663.
17. Buzsáki G, Eidelberg E (1982) Direct afferent excitation and long-term potentiation of hippocampal interneurons. J Neurophysiol 48:597-607.
18. Cobb SR, Buhl EH, Halasy K, Paulsen O, Somogyi P (1995) Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons. Nature 378:75-78.
19. Cossart R, Esclapez M, Hirsch JC, Bernard C, Ben-Ari Y (1998) GluR5 kainate receptor activation in interneurons increases tonic inhibition of pyramidal cells. Nat Neurosci 1:470-478.
20. deLanerolle NC, Kim JH, Robbins RJ, Spencer DD (1989) Hippocampal interneuron loss and plasticity in human temporal lobe epilepsy. Brain Res 495:387-395.
21. Douglas RM, McNaughton BL, Goddard GV (1983) Commissural inhibition and facilitation of granule cell discharge in fascia dentata. J Comp Neurol 219:285-294.
22. Frerking M, Malenka RC, Nicoll RA (1998) Synaptic activation of kainate receptors on hippocampal interneurons. Nat Neurosci 1:479-486.
23. Freund TF, Buzsáki G (1996) Interneurons of the hippocampus. Hippocampus 6:347-470.
24. Hampson RE, Simeral JD, Deadwyler SA (1999) Distribution of spatial and nonspatial information in dorsal hippocampus. Nature 402:610-614.
25. Hetherington PA, Austin KB, Shapiro ML (1994) Ipsilateral associational pathway in the dentate gyrus: an excitatory feedback system that supports N-methyl-D-aspartate-dependent long-term potentiation. Hippocampus 4:422-438.
26. Leranth C, Szeidemann Z, Hsu M, Buzsáki G (1996) AMPA receptors in the rat and primate hippocampus: a possible absence of GluR2/3 subunits in most interneurons. Neuroscience 70:631-652.
27. Margerison JH, Corsellis JA (1966) Epilepsy and the temporal lobes. A clinical, electroencephalographic and neuropathological study of the brain in epilepsy, with particular reference to the temporal lobes. Brain 89:499-530.
28. Melyan Z, Wheal HV, Lancaster B (2002) Metabotropic-mediated kainate receptor regulation of IsAHP and excitability in pyramidal cells. Neuron 34:107-114.
29. Milgram NW, Yearwood T, Khurgel M, Ivy GO, Racine R (1991) Changes in inhibitory processes in the hippocampus following recurrent seizures induced by systemic administration of kainic acid. Brain Res 551:236-246.
30. Monaghan DT, Cotman CW (1982) The distribution of [3H]kainic acid binding sites in rat CNS as determined by autoradiography. Brain Res 252:91-100.
31. Moser MB, Moser EI (1998) Functional differentiation in the hippocampus. Hippocampus 8:608-619.
32. Paternain AV, Herrera MT, Nieto MA, Lerma J (2000) GluR5 and GluR6 kainate receptor subunits coexist in hippocampal neurons and coassemble to form functional receptors. J Neurosci 20:196-205.
33. Paxinos G, Watson C (1998) The rat brain in stereotaxic coordinates. San Diego: Academic.
34. Qiu K, Han ZS (1995) Local projections of GABAergic neurons in the dentate gyrus and CA1 region in the rat hippocampal formation. Brain Res 702:287-292.
35. Ribak CE, Seress L, Amaral DG (1985) The development, ultrastructure and synaptic connections of the mossy cells of the dentate gyrus. J Neurocytol 14:835-857.
36. Scharfman HE (1995) Electrophysiological evidence that dentate hilar mossy cells are excitatory and innervate both granule cells and interneurons. J Neurophysiol 74:179-194.
37. Schmued LC, Fallon JH (1986) Fluoro-Gold: a new fluorescent retrograde axonal tracer with numerous unique properties. Brain Res 377:147-154.
38. Schmued LC, Hopkins KJ (2000) Fluoro-Jade B: a high affinity fluorescent marker for the localization of neuronal degeneration. Brain Res 874:123-130.
39. Sik A, Penttonen M, Buzsáki G (1997) Interneurons in the hippocampal dentate gyrus: an in vivo intracellular study. Eur J Neurosci 9:573-588.
40. Sloviter RS (1983) "Epileptic" brain damage in rats induced by sustained electrical stimulation of the perforant path. I. Acute electrophysiological and light microscopic studies. Brain Res Bull 10:675-697.
41. Sloviter RS (1987) Decreased hippocampal inhibition and a selective loss of interneurons in experimental epilepsy. Science 235:73-76.
42. SloviterRS (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.
43. Sloviter RS (1994) The functional organization of the hippocampal dentate gyrus and its relevance to the pathogenesis of temporal lobe epilepsy. Ann Neurol 35:640-654.
44. Sloviter RS, Brisman JL (1995) Lateral inhibition and granule cell synchrony in the rat hippocampal dentate gyrus. J Neurosci 15:811-820.
45. Sloviter RS, Nilaver G (1987) Immunocytochemical localization of GABA-, cholecystokinin-, vasoactive intestinal polypeptide- and somatostatin-like immunoreactivity in the area dentata and hippocampus of the rat. J Comp Neurol 256:42-60.
46. 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.
47. Soriano E, Frotscher M (1994) Mossy cells of the rat fascia dentata are glutamate-immunoreactive. Hippocampus 4:65-70.
48. Steward O, Tomasulo R, Levy WB (1990) Blockade of inhibition in a pathway with dual excitatory and inhibitory action unmasks a capability for LTP that is otherwise not expressed. Brain Res 516:292-300.
49. Struble RG, Desmond NL, Levy WB (1978) Anatomical evidence for interlamellar inhibition in the fascia dentata. Brain Res 152:580-585.
50. Sutula T, Zhang P, Lynch M, Sayin U, Golarai G, Rod R (1998) Synaptic and axonal remodeling of mossy fibers in the hilus and supragranular region of the dentate gyrus in kainate-treated rats. J Comp Neurol 390:578-594.
51. Wenzel HJ, Buckmaster PS, Anderson NL, Wenzel ME, Schwartzkroin PA (1997) Ultrastructural localization of neurotransmitter immunoreactivity in mossy cell axons and their synaptic targets in the rat dentate gyrus. Hippocampus 7:559-570.
52. Zappone CA, Sloviter RS (2001) Commissurally projecting inhibitory interneurons of the rat hippocampal dentate gyrus: a colocalization study of neuronal markers and the retrograde tracer Fluoro-Gold. J Comp Neurol 441:324-344.