Rapid Deletion of Mossy Cells Does Not Result in a Hyperexcitable Dentate Gyrus: Implications for Epileptogenesis

Journal of Neuroscience

Volumn 24, Issue 9, 2004, Pages 2259-2269

  Ratzliff, Anna D H ^a   Howard, Allyson L ^a   Santhakumar, Vijayalakshmi ^a   Osapay, Imola ^a   Soltesz, Ivan ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Dentate gyrus; Dormant basket cell hypothesis; Epilepsy; Hilar cell loss; Hyperexcitability; Mossy cell

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; 4 AMINOBUTYRIC ACID RECEPTOR BLOCKING AGENT;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN INJURY; BRAIN SLICE; CELL LOSS; CELL SPECIFICITY; CONTROLLED STUDY; DENTATE GYRUS; EPILEPSY; EPILEPTOGENESIS; GRANULE CELL; HIPPOCAMPUS; HYPOTHESIS; INTERNEURON; LAMELLAR BODY; MOSSY FIBER; NERVE CELL DEGENERATION; NERVE CELL NETWORK; NERVE EXCITABILITY; NERVE FIBER; NEUROPATHOLOGY; NEUROPIL; NONHUMAN; PRIORITY JOURNAL; RAT; SEIZURE; SYNAPSE;

DENTATE GYRUS; DISEASE MODELS, ANIMAL; ELECTRIC STIMULATION; EPILEPSY, TEMPORAL LOBE; EXCITATORY POSTSYNAPTIC POTENTIALS; GABA ANTAGONISTS; GAMMA-AMINOBUTYRIC ACID; INTERNEURONS; MOSSY FIBERS, HIPPOCAMPAL; NERVE NET; NEURONS; NEUROPIL; PATCH-CLAMP TECHNIQUES; PERFORANT PATHWAY; REACTION TIME;

EID: 1542286867     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5191-03.2004     Document Type: Article

References (55)

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, Soleng AF, Raastad M (2000) The hippocampal lamella hypothesis revisited. Brain Res 886:165-171.
4. Arabadzisz D, Freund TF (1999) Changes in excitatory and inhibitory circuits of the rat hippocampus 12-14 months after complete forebrain ischemia. Neuroscience 92:27-45.
5. Bernard C, Esclapez M, Hirsch JC, Ben Ari Y (1998) Interneurones are not so dormant in temporal lobe epilepsy: a critical reappraisal of the dormant basket cell hypothesis. Epilepsy Res 32:93-103.
6. Blasco-Ibanez JM, Freund TF (1997) Distribution, ultrastructure, and connectivity of calretinin-immunoreactive mossy cells of the mouse dentate gyrus. Hippocampus 7:307-320.
7. 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.
8. Brooks-Kayal AR, Shumate MD, Jin H, Rikhter TY, Kelly ME, Coulter DA (2001) gamma-Aminobutyric acid(A) receptor subunit expression predicts functional changes in hippocampal dentate granule cells during postnatal development. J Neurochem 77:1266-1278.
9. Buckmaster PS, Dudek FE (1999) In vivo intracellular analysis of granule cell axon reorganization in epileptic rats. J Neurophysiol 81:712-721.
10. Buckmaster PS, Jongen-Relo AL (1999) Highly specific neuron loss preserves lateral inhibitory circuits in the dentate gyrus of kainate-induced epileptic rats. J Neurosci 19:9519-9529.
11. Buckmaster PS, Strowbridge BW, Kunkel DD, Schmiege DL, Schwartzkroin PA (1992) Mossy cell axonal projections to the dentate gyrus molecular layer in the rat hippocampal slice. Hippocampus 2:349-362.
12. 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.
13. Cavazos JE, Das I, Sutula TP (1994) Neuronal loss induced in limbic pathways by kindling: evidence for induction of hippocampal sclerosis by repeated brief seizures. J Neurosci 14:3106-3121.
14. Freund TF, Buzsaki G (1996) Interneurons of the hippocampus. Hippocampus 6:347-470.
15. Frotscher M, Seress L, Schwerdtfeger WK, Buhl E (1991) The mossy cells of the fascia dentata: a comparative study of their fine structure and synaptic connections in rodents and primates. J Comp Neurol 312:145-163.
16. Gaugain B, Barbet J, Capelle N, Roques BP, Le Pecq JB (1978) DNA Bifunctional intercalators. 2. Fluorescence properties and DNA binding interaction of an ethidium homodimer and an acridine ethidium heterodimer. Biochemistry 17:5078-5088.
17. Geiger JR, Lubke J, Roth A, Frotscher M, Jonas P (1997) Submillisecond AMPA receptor-mediated signaling at a principal neuron-interneuron synapse. Neuron 18:1009-1023.
18. Gulyas AI, Miles R, Sik A, Toth K, Tamamaki N, Freund TF (1993) Hippocampal pyramidal cells excite inhibitory neurons through a single release site. Nature 366:683-687.
19. Hajos N, Mody I (1997) Synaptic communication among hippocampal interneurons: properties of spontaneous IPSCs in morphologically identified cells. J Neurosci 17:8427-8442.
20. Haugland R (1996) Assays for cell viability, proliferation and function. In: Molecular probes handbook of fluorescent probes and research chemicals (Spence M, ed), pp 366-398. Eugene, OR: Molecular Probes.
21. Hollrigel GS, Toth K, Soltesz I (1996) Neuroprotection by propofol in acute mechanical injury: role of GABAergic inhibition. J Neurophysiol 76:2412-2422.
22. Houser CR (1999) Neuronal loss and synaptic reorganization in temporal lobe epilepsy. Adv Neurol 79:743-761.
23. Ishizuka S, Kosaka T (1998) Physiological properties of mouse hippocampal mossy cells. NeuroReport 9:193-199.
24. Kapur J (2000) Hippocampal neurons express GABA A receptor insensitive to diazepam in hyperexcitable conditions. Epilepsia 41 [Suppl 6]:S86-S89.
25. Kotti T, Tapiola T, Riekkinen Sr PJ, Miettinen R (1996) The calretinin-containing mossy cells survive excitotoxic insult in the gerbil dentate gyrus. Comparison of excitotoxicity-induced neuropathological changes in the gerbil and rat. Eur J Neurosci 8:2371-2378.
26. Kraushaar U, Jonas P (2000) Efficacy and stability of quantal GABA release at a hippocampal interneuron-principal neuron synapse. J Neurosci 20:5594-5607.
27. Lechner HA, Lein ES, Callaway EM (2002) A genetic method for selective and quickly reversible silencing of mammalian neurons. J Neurosci 22:5287-5290.
28. Leranth C, Szeidemann Z, Hsu M, Buzsaki G (1996) AMPA receptors in the rat and primate hippocampus: a possible absence of GluR2/3 subunits in most interneurons. Neuroscience 70:631-652.
29. Liu KS, Fetcho JR (1999) Laser ablations reveal functional relationships of segmental hindbrain neurons in zebrafish. Neuron 23:325-335.
30. Lowenstein DH, Thomas MJ, Smith DH, McIntosh TK (1992) Selectivevulnerability 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.
31. Monette R, Small DL, Mealing G, Morley P (1998) A fluorescence confocal assay to assess neuronal viability in brain slices. Brain Res Brain Res Protoc 2:99-108.
32. Patton PE, McNaughton B (1995) Connection matrix of the hippocampal formation: I. The dentate gyrus. Hippocampus 5:245-286.
33. Ratzliff AD, 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.
34. Ratzliff AH, Santhakumar V, Howard A, Soltesz I (2002) Mossy cells in epilepsy: rigor mortis or vigor mortis? Trends Neurosci 25:140-144.
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. Ribak CE, Seress L, Peterson GM, Seroogy KB, Fallon JH, Schmued LC (1986) A GABAergic inhibitory component within the hippocampal commissural pathway. J Neurosci 6:3492-3498.
37. Ross ST, Soltesz I (2000) Selective depolarization of interneurons in the early posttraumatic dentate gyrus: involvement of the Na(+)/K(+)-ATPase. J Neurophysiol 83:2916-2930.
38. Santhakumar V, Bender R, Frotscher M, Ross ST, Hollrigel GS, Toth Z, Soltesz I (2000) Granule cell hyperexcitability in the early posttraumatic rat dentate gyrus: the "irritable mossy cell" hypothesis. J Physiol 524:117-134.
39. Santhakumar V, Ratzliff AD, Jeng J, Toth K, Soltesz I (2001) Long-term hyperexcitability in the hippocampus after experimental head trauma. Ann Neurol 50:708-717.
40. Scharfman HE (1991) Dentate hilar cells with dendrites in the molecular layer have lower thresholds for synaptic activation by perforant path than granule cells. J Neurosci 11:1660-1673.
41. Scharfman HE (1995) Electrophysiological evidence that dentate hilar mossy cells are excitatory and innervate both granule cells and interneurons. J Neurophysiol 74:179-194.
42. Shah EM, Iay DG (1993) Methods for ablating neurons. Curr Opin Neurobiol 3:738-742.
43. 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.
44. 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.
45. 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.
46. Soltesz I, Bourassa J, Deschenes M (1993) The behavior of mossy cells of the rat dentate gyrus during theta oscillations in vivo. Neuroscience 57:555-564.
47. Sutula T, He XX, Cavazos J, Scott G (1988) Synaptic reorganization in the hippocampus induced by abnormal functional activity. Science 239:1147-1150.
48. Tauck DL, Nadler JV (1985) Evidence of functional mossy fiber sprouting in hippocampal formation of kainic acid-treated rats. J Neurosci 5:1016-1022.
49. Toth K, McBain CJ (1998) Afferent-specific innervation of two distinct AMPA receptor subtypes on single hippocampal interneurons. Nat Neurosci 1:572-578.
50. Toth Z, Hollrigel GS, Gorcs T, Soltesz I (1997) Instantaneous perturbation of dentate interneuronal networks by a pressure wave-transient delivered to the neocortex. J Neurosci 17:8106-8117.
51. Wang X, Lambert NA (2003) Membrane properties of identified lateral and medial perforant pathway projection neurons. Neuroscience 117:485-492.
52. 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.
53. Westbrook GL (2000) Seizures and epilepsy. In: Principles of neural science (Kandel ER, Schwartz JH, Jessell TM, eds), pp 910-935. New York: McGraw-Hill.
54. Wuarin JP, Dudek FE (2001) Excitatory synaptic input to granule cells increases with time after kainate treatment. J Neurophysiol 85:1067-1077.
55. 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.