Enhanced excitatory synaptic connectivity in layer V pyramidal neurons of chronically injured epileptogenic neocortex in rats

Journal of Neuroscience

Volumn 26, Issue 18, 2006, Pages 4891-4900

  Jin, Xiaoming ^a   Prince, David A ^a   Huguenard, John R ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Caged compound; Electrophysiology; Epilepsy; Excitability; Neocortex; Synaptic transmission

Indexed keywords

2 AMINO 5 PHOSPHONOVALERIC ACID; GLUTAMIC ACID; ALPHA (4,5 DIMETHOXY 2 NITROBENZYL) GLUTAMATE; ALPHA-(4,5-DIMETHOXY-2-NITROBENZYL) GLUTAMATE; AMINO ACID RECEPTOR BLOCKING AGENT; BIOCYTIN; DRUG DERIVATIVE; GLUTAMIC ACID DERIVATIVE; LOCAL ANESTHETIC AGENT; LYSINE; TETRODOTOXIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EPILEPSY; EPILEPTOGENESIS; NEOCORTEX; NERVE EXCITABILITY; NONHUMAN; PATCH CLAMP; PHOTOSTIMULATION; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SOMATOSENSORY CORTEX; SYNAPTIC TRANSMISSION; ANALYSIS OF VARIANCE; ANIMAL; BRAIN INJURY; BRAIN MAPPING; CELL COUNT; COMPARATIVE STUDY; CONFOCAL MICROSCOPY; DRUG EFFECT; ELECTROSTIMULATION; EXCITATORY POSTSYNAPTIC POTENTIAL; IN VITRO STUDY; INJURY; METHODOLOGY; NEWBORN; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; RADIATION EXPOSURE; SPRAGUE DAWLEY RAT;

2-AMINO-5-PHOSPHONOVALERATE; ANALYSIS OF VARIANCE; ANESTHETICS, LOCAL; ANIMALS; ANIMALS, NEWBORN; BRAIN INJURIES; BRAIN MAPPING; CELL COUNT; ELECTRIC STIMULATION; EXCITATORY AMINO ACID ANTAGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; GLUTAMATES; LYSINE; MICROSCOPY, CONFOCAL; PATCH-CLAMP TECHNIQUES; PHOTIC STIMULATION; PYRAMIDAL CELLS; RATS; RATS, SPRAGUE-DAWLEY; SOMATOSENSORY CORTEX; SYNAPTIC TRANSMISSION; TETRODOTOXIN;

EID: 33646945321     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4361-05.2006     Document Type: Article

References (82)

1. Annegers JF, Grabow JD, Groover RV, Laws Jr ER, Elveback LR, Kurland LT (1980) Seizures after head trauma: a population study. Neurology 30:683-689.
2. Bacci A, Rudolph U, Huguenard JR, Prince DA (2003) Major differences in inhibitory synaptic transmission onto two neocortical interneuron subclasses. J Neurosci 23:9664-9674.
3. Bernard C, Esclapez M, Hirsch JC, Ben-Ari Y (1998) Interneurons are not so dormant in temporal lobe epilepsy: a critical reappraisal of the dormant basket cell hypothesis. Epilepsy Res 32:93-103.
4. 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.
5. 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.
6. Callaway EM (2002) Cell type specificity of local cortical connections. J Neurocytol 31:231-237.
7. Callaway EM, Katz LC (1993) Photostimulation using caged glutamate reveals functional circuitry in living brain slices. Proc Natl Acad Sci USA 90:7661-7665.
8. Carmichael ST (2003) Plasticity of cortical projections after stroke. Neuroscientist 9:64-75.
9. Carmichael ST, Wei L, Rovainen CM, Woolsey TA (2001) New patterns of intra-cortical projections after focal cortical stroke. Neurobiol Dis 8:910-922.
10. Chagnac-Amitai Y, Connors BW (1989) Horizontal spread of synchronized activity in neocortex and its control by GABA-mediated inhibition. J Neurophysiol 61:747-758.
11. Chuckowree JA, Dickson TC, Vickers JC (2004) Intrinsic regenerative ability of mature CNS neurons. Neuroscientist 10:280-285.
12. Cossart R, Bernard C, Ben Ari Y (2005) Multiple facets of GABAergic neurons and synapses: multiple fates of GABA signalling in epilepsies. Trends Neurosci 28:108-115.
13. Dantzker JL, Callaway EM (2000) Laminar sources of synaptic input to cortical inhibitory interneurons and pyramidal neurons. Nat Neurosci 3:701-707.
14. Destexhe A, Pare D (1999) Impact of network activity on the integrative properties of neocortical pyramidal neurons in vivo. J Neurophysiol 81:1531-1547.
15. Dodt HU, Schierloh A, Eder M, Zieglgansberger W (2003) Circuitry of rat barrel cortex investigated by infrared-guided laser stimulation. NeuroReport 14:623-627.
16. Dudek FE, Spitz M (1997) Hypothetical mechanisms for the cellular and neurophysiologic basis of secondary epileptogenesis: proposed role of synaptic reorganization. J Clin Neurophysiol 14:90-101.
17. 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.
18. Fishman PS, Mattu A (1993) Fate of severed cortical projection axons. J Neurotrauma 10:457-470.
19. Franck JE, Kunkel DD, Baskin DG, Schwartzkroin PA (1988) Inhibition in kainate-lesioned hyperexcitable hippocampi: physiologic, autoradiographic and immunocytochemical observations. J Neurosci 8:1991-2002.
20. Golarai G, Greenwood AC, Feeney DM, Connor JA (2001) Physiological and structural evidence for hippocampal involvement in persistent seizure susceptibility after traumatic brain injury. J Neurosci 21:8523-8537.
21. Graber KD, Prince DA (1999) Tetrodotoxin prevents posttraumatic epileptogenesis in rats. Ann Neurol 46:234-242.
22. Graber KD, Prince DA (2006) Chronic partial cortical isolation. In: Models of seizures and epilepsy (Pitkanen A, Schwartzkroin P, Moshe S, eds), pp 477-493. San Diego: Elsevier.
23. Graber KD, Kharazia VN, Parada I, Prince DA (1999) Parvalbumin containing interneurons are spared in the undercut model of posttraumatic epileptogenesis. Epilepsia 40 [Suppl 7]:31.
24. Hoffman SN, Salin PA, Prince DA (1994) Chronic neocortical epileptogenesis in vitro. J Neurophysiol 71:1762-1773.
25. Horikawa K, Armstrong WE (1988) A versatile means of intracellular labeling: injection of biocytin and its detection with avidin conjugates. J Neurosci Methods 25:1-11.
26. - extrusion in layer V pyramidal neurons of chronically injured epileptogenic neocortex. J Neurophysiol 93:2117-2126.
27. Jin X, Huguenard JR, Prince DA (2005b) Increased layer V excitatory connectivity in the neocortical undercut model of post-traumatic epilepsy. Epilepsia 46 [Suppl 8]:109.
28. Katz LC, Dalva MB (1994) Scanning laser photostimulation: a new approach for analyzing brain circuits. J Neurosci Methods 54:205-218.
29. Kittelberger JM, Mooney R (1999) Lesions of an avian forebrain nucleus that disrupt song development alter synaptic connectivity and transmission in the vocal premotor pathway. J Neurosci 19:9385-9398.
30. Kobayashi M, Wen X, Buckmaster PS (2003) Reduced inhibition and increased output of layer II neurons in the medial entorhinal cortex in a model of temporal lobe epilepsy. J Neurosci 23:8471-8479.
31. Kotter R, Staiger JF, Zilles K, Luhmann HJ (1998) Analyzing functional connectivity in brain slices by a combination of infrared video microscopy, flash photolysis of caged compounds and scanning methods. Neuroscience 86:265-277.
32. Kotti T, Riekkinen PJ, Miettinen R (1997) Characterization of target cells for aberrant mossy fiber collaterals in the dentate gyrus of epileptic rat. Exp Neurol 146:323-330.
33. Lee JK, Kim JE, Sivula M, Strittmatter SM (2004) Nogo receptor antagonism promotes stroke recovery by enhancing axonal plasticity. J Neurosci 24:6209-6217.
34. 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.
35. Li H, Prince DA (2002) Synaptic activity in chronically injured, epileptogenic sensory-motor neocortex. J Neurophysiol 88:2-12.
36. Longo BM, Mello LE (1997) Blockade of pilocarpine- or kainate-induced mossy fiber sprouting by cycloheximide does not prevent subsequent epileptogenesis in rats. Neurosci Lett 226:163-166.
37. Lynch M, Sutula T (2000) Recurrent excitatory connectivity in the dentate gyrus of kindled and kainic acid-treated rats. J Neurophysiol 83:693-704.
38. Marchenko VG, Pasikova NV, Kositsyn NS (2004) Intracortical synchronization of epileptic discharges at different stages of ultrastructural rearrangements in a completely neuronally isolated area of rat neocortex. Neurosci Behav Physiol 34:307-313.
39. Markram H, Lubke J, Frotscher M, Roth A, Sakmann B (1997) Physiology and anatomy of synaptic connections between thick tufted pyramidal neurones in the developing rat neocortex. J Physiol (Lond) 500:409-440.
40. Maxwell WL, Follows R, Ashhurst DE, Berry M (1990) The response of the cerebral hemisphere of the rat to injury. I. The mature rat. Philos Trans R Soc Lond B Biol Sci 328:479-500.
41. McKinney RA, Debanne D, Gahwiler BH, Thompson SM (1997) Lesion-induced axonal sprouting and hyperexcitability in the hippocampus in vitro: implications for the genesis of posttraumatic epilepsy. Nat Med 3:990-996.
42. Molnar P, Nadler JV (1999) Mossy fiber-granule cell synapses in the normal and epileptic rat dentate gyrus studied with minimal laser photostimulation. J Neurophysiol 82:1883-1894.
43. Nadler JV (2003) The recurrent mossy fiber pathway of the epileptic brain. Neurochem Res 28:1649-1658.
44. Okazaki MM, Molnar P, Nadler JV (1999) Recurrent mossy fiber pathway in rat dentate gyrus: synaptic currents evoked in the presence and absence of seizure-induced growth. J Neurophysiol 81:1645-1660.
45. Patrylo PR, Dudek FE (1998) Physiological unmasking of new glutamatergic pathways in the dentate gyrus of hippocampal slices from kainate-induced epileptic rats. J Neurophysiol 79:418-429.
46. Perez Y, Morin F, Beaulieu C, Lacaille J-C (1996) Axonal sprouting of CA1 pryamidal cells in hyperexcitable hippocampal slices of kainate-treated rats. Eur J Neurosci 8:736-748.
47. Prince DA (1999) Epileptogenic neurons and circuits. Adv Neurol 79:665-684.
48. Prince DA, Tseng GF (1993) Epileptogenesis in chronically injured cortex: in vitro studies. J Neurophysiol 69:1276-1291.
49. Prince DA, Salin P, Tseng GF, Hoffman S, Parada I (1997) Axonal sprouting and epileptogenesis. Adv Neurol 72:1-8.
50. Purpura DP, Housepian EM (1961) Morphological and physiological properties of chronically isolated immature neocortex. Exp Neurol 4:377-401.
51. Ramirez JJ (2001) The role of axonal sprouting in functional reorganization after CNS injury: lessons from the hippocampal formation. Restor Neurol Neurosci 19:237-262.
52. Ribak CE, Harris AB, Vaughn JE, Roberts E (1979) Inhibitory, GABAergic nerve terminals decrease at sites of focal epilepsy. Science 205:211-214.
53. Ribak CE, Bradurne RM, Harris AB (1982) A preferential loss of GABAergic, symmetric synapses in epileptic foci: a quantitative ultrastructural analysis of monkey neocortex. J Neurosci 2:1725-1735.
54. Rice A, Rafiq A, Shapiro SM, Jakoi ER, Coulter DA, Delorenzo RJ (1996) Long-lasting reduction of inhibitory function and γ-aminobutyric acid type A receptor subunit mRNA expression in a model of temporal lobe epilepsy. Proc Natl Acad Sci USA 93:9665-9669.
55. Salin P, Tseng G-F, Salin P, Hoffman S, Parada I, Prince DA (1995) Axonal sprouting in layer V pyramidal neurons of chronically injured cerebral cortex. J Neurosci 15:8234-8245.
56. 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.
57. Scharfman HE, Sollas AL, Berger RE, Goodman JH (2003) Electrophysiological evidence of monosynaptic excitatory transmission between granule cells after seizure-induced mossy fiber sprouting. J Neurophysiol 90:2536-2547.
58. Schubert D, Staiger JF, Cho N, Kötter R, Zilles K, Luhmann HJ (2001) Layer-specific intracolumnar and transcolumnar functional connectivity of layer V pyramidal cells in rat barrel cortex. J Neurosci 21:3580-3592.
59. Shao LR, Dudek FE (2004) Increased excitatory synaptic activity and local connectivity of hippocampal CA1 pyramidal cells in rats with kainateinduced epilepsy. J Neurophysiol 92:1366-1373.
60. Shepherd GMG, Svoboda K (2005) Laminar and columnar organization of ascending excitatory projections to layer 2/3 pyramidal neurons in rat barrel cortex. J Neurosci 25:5670-5679.
61. Shepherd GMG, Pologruto TA, Svoboda K (2003) Circuit analysis of experience-dependent plasticity in the developing rat barrel cortex. Neuron 38:277-289.
62. Sloviter RS (1987) Decreased hippocampal inhibition and a selective loss of interneurons in experimental epilepsy. Science 235:73-76.
63. Sloviter RS (1992) Possible functional consequences of synaptic reorganization in the dentate gyrus of kainate-treated rats. Neurosci Lett 137:91-96.
64. Smith BN, Dudek FE (2002) Network interactions mediated by new excitatory connections between CA1 pyramidal cells in rats with kainite-induced epilepsy. J Neurophysiol 87:1655-1658.
65. Staiger JF, Kotter R, Zilles K, Luhmann HJ (2000) Laminar characteristics of functional connectivity in rat barrel cortex revealed by stimulation with caged-glutamate. Neurosci Res 37:49-58.
66. Stroemer RP, Kent TA, Hulsebosch CE (1998) Enhanced neocortical neural sprouting, synaptogenesis, and behavioral recovery with D-Amphetamine therapy after neocortical infarction in rats. Stroke 29:2381-2395.
67. 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.
68. Sutula TP, Golarai G, Cavazos J (1992) Assessing the functional significance of mossy fiber sprouting. Epilepsy Res Suppl 7:251-259.
69. Tauck DL, Nadler JV (1985) Evidence of functional mossy fiber sprouting in hippocampal formation of kainic acid treated rats. J Neurosci 5:1016-1022.
70. Traub RD, Wong RK (1982) Cellular mechanism of neuronal synchronization in epilepsy. Science 216:745-747.
71. Tsai PS, Nishimura N, Yoder EJ, White A, Dolnick E, Kleinfeld D (2002) Principles, design and construction of a two photon scanning microscope for in vitro and in vivo studies. In: Methods for in vivo optical imaging (Frostig R, ed), pp 113-171. Boca Raton, FL: CRC.
72. Tseng GF, Prince DA (1996) Structural and functional alterations in rat corticospinal neurons after axotomy. J Neurophysiol 75:248-267.
73. Tseng GF, Parada I, Prince DA (1991) Double-labelling with rhodamine beads and biocytin: a technique for studying corticospinal and other projection neurons in vitro. J Neurosci Methods 37:121-131.
74. B receptor-mediated responses in GABAergic projection neurones of rat nucleus reticularis thalami in vitro. J Physiol (Lond) 493:845-854.
75. Wei DS, Mei YA, Bagal A, Kao JPY, Thompson SM, Tang CM (2001) Compartmentalized and binary behavior of terminal dendrites in hippocampal pyramidal neurons. Science 293:2272-2275.
76. Wenzel HJ, Woolley CS, Robbins CA, Schwartzkroin PA (2000) Kainic acid-induced mossy fiber sprouting and synapse formation in the dentate gyrus of rats. Hippocampus 10:244-260.
77. Wong RK, Miles R, Traub RD (1984) Local circuit interactions in synchronization of cortical neurones. J Exp Biol 112:169-178.
78. Wuarin JP, Dudek FE (1996) Electrographic seizures and new recurrent excitatory circuits in the dentate gyrus of hippocampal slices from kainate-treated epileptic rats. J Neurosci 16:4438-4448.
79. Wuarin JP, Dudek FE (2001) Excitatory synaptic input to granule cells increases with time after kainate treatment. J Neurophysiol 85:1067-1077.
80. Xiang Z, Huguenard JR, Prince DA (2002) Synaptic inhibition of pyramidal cells evoked by different interneuronal subtypes in layer V of rat visual cortex. J Neurophysiol 88:740-750.
81. Zhang N, Houser CR (1999) Ultrastructural localization of dynorphin in the dentate gyrus in human temporal lobe epilepsy: a study of reorganized mossy fiber synapses. J Comp Neurol 405:472-490.
82. Zhu WJ, Roper SN (2000) Reduced inhibition in an animal model of cortical dysplasia. J Neurosci 20:8925-8931.