Cortical excitation and inhibition following focal traumatic brain injury

Journal of Neuroscience

Volumn 31, Issue 40, 2011, Pages 14085-14094

  Ding, Ming Chieh ^a,b   Wang, Qi ^d   Lo, Eng H ^c   Stanley, Garrett B ^d  

^a HARVARD UNIVERSITY   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN CORTEX INHIBITION; CONTROLLED STUDY; CORTICAL EXCITATION; EVOKED SOMATOSENSORY RESPONSE; HYPEREXCITABILITY; IN VIVO STUDY; INJURY SEVERITY; MALE; NERVOUS SYSTEM FUNCTION; NONHUMAN; PRIORITY JOURNAL; RAT; SOMATOSENSORY CORTEX; TACTILE STIMULATION; THALAMOCORTICAL TRACT; TRAUMATIC BRAIN INJURY; VIBRISSA;

ANIMALS; BRAIN INJURIES; MALE; NEURAL INHIBITION; PHYSICAL STIMULATION; RATS; RATS, LONG-EVANS; SOMATOSENSORY CORTEX; TIME FACTORS; VIBRISSAE;

EID: 80053633061     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3572-11.2011     Document Type: Article

References (89)

1. Adamo PF, Crawford JT, Stepien RL (2005) Subdural hematoma of the brainstem in a dog: magnetic resonance findings and treatment. J Am Anim Hosp Assoc 41:400-405.
2. Ahissar E, Zacksenhouse M (2001) Temporal and spatial coding in the rat vibrissal system. Prog Brain Res 130:75-87.
3. Alves OL, Bullock R, Clausen T, Reinert M, Reeves TM (2005) Concurrent monitoring of cerebral electrophysiology and metabolism after traumatic brain injury: an experimental and clinical study. J Neurotrauma 22:733-749.
4. Andermann ML, Moore CI (2006) A somatotopic map of vibrissa motion direction within a barrel column. Nat Neurosci 9:543-551.
5. Armstrong-James M, Fox K, Das-Gupta A (1992) Flow of excitation within rat barrel cortex on striking a single vibrissa. J Neurophysiol 68:1345-1358.
6. Aronoff R, Matyas F, Mateo C, Ciron C, Schneider B, Petersen CC (2010) Long-range connectivity of mouse primary somatosensory barrel cortex. Eur J Neurosci 31:2221-2233.
7. Arundine M, Tymianski M (2004) Molecular mechanisms of glutamate-dependent neurodegeneration in ischemia and traumatic brain injury. Cell Mol Life Sci 61:657-668.
8. Arundine M, Chopra GK, Wrong A, Lei S, Aarts MM, MacDonald JF, Tymi-anski M (2003) Enhanced vulnerability to NMDA toxicity in sublethal traumatic neuronal injury in vitro. J Neurotrauma 20:1377-1395.
9. Avramescu S, Timofeev I (2008) Synaptic strength modulation after cortical trauma: a role in epileptogenesis. J Neurosci 28:6760-6772.
10. Baker AJ, Park E, Hare GM, Liu E, Sikich N, Mazer DC (2008) Effects of resuscitation fluid on neurologic physiology after cerebral trauma and hemorrhage. J Trauma 64:348-357.
11. Berger M, Speckmann EJ, Pape HC, Gorji A (2008) Spreading depression enhances human neocortical excitability in vitro. Cephalalgia 28:558 -562.
12. Boloori AR, Stanley GB (2006) The dynamics of spatiotemporal response integration in the somatosensory cortex of the vibrissa system. J Neurosci 26:3767-3782.
13. Boloori AR, Jenks RA, Desbordes G, Stanley GB (2010) Encoding and decoding cortical representations of tactile features in the vibrissa system. J Neurosci 30:9990-10005.
14. Bonislawski DP, Schwarzbach EP, Cohen AS (2007) Brain injury impairs dentate gyrus inhibitory efficacy. Neurobiol Dis 25:163-169.
15. Chen JR, Wang YJ, Tseng GF (2004) The effects of decompression and exogenous NGF on compressed cerebral cortex. J Neurotrauma 21:1640-1651.
16. Chung S, Li X, Nelson SB (2002) Short-term depression at thalamocortical synapses contributes to rapid adaptation of cortical sensory responses in vivo. Neuron 34:437-446.
17. Church AJ, Andrew RD (2005) Spreading depression expands traumatic injury in neocortical brain slices. J Neurotrauma 22:277-290.
18. Clarkson AN, Huang BS, Macisaac SE, Mody I, Carmichael ST (2010) Reducing excessive GABA-mediated tonic inhibition promotes functional recovery after stroke. Nature 468:305-309.
19. Cohen AS, Pfister BJ, Schwarzbach E, Grady MS, Goforth PB, Satin LS (2007) Injury-induced alterations in CNS electrophysiology. Prog Brain Res 161:143-169.
20. David-Jürgens M, Dinse HR (2010) Effects of aging on paired-pulse behavior of rat somatosensory cortical neurons. Cereb Cortex 20:1208-1216.
21. Desîlets-Roy B, Varga C, Lavallée P, Deschênes M (2002) Substrate for cross-talk inhibition between thalamic barreloids. J Neurosci 22:RC218.
22. Dijkhuizen RM, Ren J, Mandeville JB, Wu O, Ozdag FM, Moskowitz MA, Rosen BR, Finklestein SP (2001) Functional magnetic resonance imaging of reorganization in rat brain after stroke. Proc Natl Acad Sci USA 98:12766-12771.
23. Dijkhuizen RM, Singhal AB, Mandeville JB, Wu O, Halpern EF, Finklestein SP, Rosen BR, Lo EH (2003) Correlation between brain reorganization, ischemic damage, and neurologic status after transient focal cerebral ischemia in rats: a functional magnetic resonance imaging study. J Neurosci 23:510-517.
24. Ding MC, Lo EH, Stanley GB (2008) Sustained focal cortical compression reduces electrically-induced seizure threshold. Neuroscience 154:551-555.
25. Ebner FF, Armstrong-James MA (1990) Intracortical processes regulating the integration of sensory information. Prog Brain Res 86:129-141.
26. Eikermann-Haerter K, Moskowitz MA (2008) Animal models of migraine headache and aura. Curr Opin Neurol 21:294-300.
27. Fanselow EE, Nicolelis MA (1999) Behavioral modulation of tactile responses in the rat somatosensory system. J Neurosci 19:7603-7616.
28. Fox K (2002) Anatomical pathways and molecular mechanisms for plasticity in the barrel cortex. Neuroscience 111:799-814.
29. Fox K, Wright N, Wallace H, Glazewski S (2003) The origin of cortical surround receptive fields studied in the barrel cortex. J Neurosci 23:8380-8391.
30. Fujioka H, Kaneko H, Suzuki SS, Mabuchi K (2004) Hyperexcitability-associated rapid plasticity after a focal cerebral ischemia. Stroke 35:e346-348.
31. Gil Z, Connors BW, Amitai Y (1997) Differential regulation of neocortical synapses by neuromodulators and activity. Neuron 19:679-686.
32. Glass TF, Reeves B, Sharp FR (2004) The impact of excitotoxic blockade on the evolution of injury following combined mechanical and hypoxic insults in primary rat neuronal culture. Neurobiol Dis 17:378-384.
33. Harris RM, Hendrickson AE (1987) Local circuit neurons in the rat ventro-basal thalamus-a GABA immunocytochemical study. Neuroscience 21:229-236.
34. Hartings JA, Strong AJ, Fabricius M, Manning A, Bhatia R, Dreier JP, Mazzeo AT, Tortella FC, Bullock MR (2009) Spreading depolarizations and late secondary insults after traumatic brain injury. J Neurotrauma 26:1857-1866.
35. Higley MJ, Contreras D (2003) Nonlinear integration of sensory responses in the rat barrel cortex: an intracellular study in vivo. J Neurosci 23:10190-10200.
36. Higley MJ, Contreras D (2006) Balanced excitation and inhibition determine spike timing during frequency adaptation. J Neurosci 26:448-457.
37. Jefferys JG (2003) Models and mechanisms of experimental epilepsies. Epi-lepsia 44 [Suppl 12]:44-50.
38. Kim DS, Ronen I, Olman C, Kim SG, Ugurbil K, Toth LJ (2004) Spatial relationship between neuronal activity and BOLD functional MRI. Neu-roimage 21:876-885.
39. Kim YR, Huang IJ, Lee SR, Tejima E, Mandeville JB, van Meer MP, Dai G, Choi YW, Dijkhuizen RM, Lo EH, Rosen BR (2005) Measurements of BOLD/CBV ratio show altered fMRI hemodynamics during stroke recovery in rats. J Cereb Blood Flow Metab 25:820-829.
40. Koistinaho J, Chan PH (2000) Spreading depression-induced cyclooxygenase-2 expression in the cortex. Neurochem Res 25:645-651.
41. Kwegyir-Afful EE, Simons DJ (2009) Subthreshold receptive field properties distinguish different classes of corticothalamic neurons in the so-matosensory system. J Neurosci 29:964-972.
42. Kyriazi HT, Carvell GE, Brumberg JC, Simons DJ (1996) Quantitative effects of GABA and bicuculline methiodide on receptive field properties of neurons in real and simulated whisker barrels. J Neurophysiol 75:547-560.
43. Kyriazi H, Carvell GE, Brumberg JC, Simons DJ (1998) Laminar differences in bicuculline methiodide's effects on cortical neurons in the rat whisker/ barrel system. Somatosens Mot Res 15:146-156.
44. Larrosa B, Pastor J, López-Aguado L, Herreras O (2006) A role for gluta-mate and glia in the fast network oscillations preceding spreading depression. Neuroscience 141:1057-1068.
45. Lee KR, Drury I, Vitarbo E, Hoff JT (1997) Seizures inducedbyintracerebral injection of thrombin: a model of intracerebral hemorrhage. J Neurosurg 87:73-78.
46. Longoni M, Ferrarese C (2006) Inflammation and excitotoxicity: role in migraine pathogenesis. Neurol Sci 27 [Suppl 2]:S107-S110.
47. Maeda M, Miyazaki M (1998) Control of ICP and the cerebrovascular bed by the cholinergic basal forebrain. Acta Neurochir Suppl 71:293-296.
48. Manor T, Barbiro-Michaely E, Rogatsky G, Mayevsky A (2008) Real-time multi-site multi-parametric monitoring of rat brain subjected to traumatic brain injury. Neurol Res 30:1075-1083.
49. Marino R, Gasparotti R, Pinelli L, Manzoni D, Gritti P, Mardighian D, La-tronico N (2006) Posttraumatic cerebral infarction in patients with moderate or severe head trauma. Neurology 67:1165-1171.
50. Maxwell WL, Watt C, Graham DI, Gennarelli TA (1993) Ultrastructural evidence ofaxonal shearing as a resultof lateral acceleration of the head in non-human primates. Acta Neuropathol 86:136-144.
51. Maxwell WL, Povlishock JT, Graham DL (1997) A mechanistic analysis of nondisruptive axonal injury: a review. J Neurotrauma 14:419-440.
52. Miller KD, Pinto DJ, Simons DJ (2001) Processing in layer 4 of the neocor-tical circuit: new insights from visual and somatosensory cortex. Curr Opin Neurobiol 11:488-497.
53. Misonou H, Mohapatra DP, Menegola M, Trimmer JS (2005) Calcium- and metabolic state-dependent modulation of the voltage-dependent Kv2.1 channel regulates neuronal excitability in response to ischemia. J Neuro-sci 25:11184-11193.
54. Moore CI, Nelson SB (1998) Spatio-temporal subthreshold receptive fields in the vibrissa representationof rat primary somatosensory cortex. J Neu-rophysiol 80:2882-2892.
55. Moreira T, Cebers G, Pickering C, Ostenson CG, Efendic S, Liljequist S (2007) Diabetic Goto-Kakizaki rats display pronounced hyperglycemia and longer-lasting cognitive impairments following ischemia induced by cortical compression. Neuroscience 144:1169-1185.
56. Petersen CC (2007) The functional organization of the barrel cortex. Neuron 56:339-355.
57. Pinault D, Bourassa J, Deschênes M (1995) The axonal arborization of single thalamic reticular neurons in the somatosensory thalamus of the rat. Eur J Neurosci 7:31-40.
58. Porter JT, Nieves D (2004) Presynaptic GABAB receptors modulate tha-lamic excitation of inhibitory and excitatory neurons in the mouse barrel cortex. J Neurophysiol 92:2762-2770.
59. Reinert M, Khaldi A, Zauner A, Doppenberg E, Choi S, Bullock R (2000) High extracellular potassium and its correlates after severe head injury: relationship to high intracranial pressure. Neurosurg Focus 8:e10.
60. Salci K, Nilsson P, Goiny M, Contant C, Piper I, Enblad P (2006) Low in-tracranial compliance increases the impact of intracranial volume insults to the traumatized brain: a microdialysis study in a traumatic brain injury rodent model. Neurosurgery 59:367-373.
61. Sanders MJ, Dietrich WD, Green EJ (2001) Behavioral, electrophysiologi-cal, and histopathological consequences of mild fluid-percussion injury in the rat. Brain Res 904:141-144.
62. Sato TR, Svoboda K (2010) The functional properties of barrel cortex neurons projecting to the primary motor cortex. J Neurosci 30:4256-4260.
63. Silver IA, Erecińska M (1994) Extracellular glucose concentration in mammalian brain: continuous monitoring of changes during increased neu-ronal activity and upon limitation in oxygen supply in normo-, hypo-, and hyperglycemic animals. J Neurosci 14:5068-5076.
64. Simons DJ (1985) Temporal and spatial integration in the rat SI vibrissa cortex. J Neurophysiol 54:615-635.
65. Simons DJ, Carvell GE (1989) Thalamocortical response transformation in the rat vibrissa/barrel system. J Neurophysiol 61:311-330.
66. Simons DJ, Woolsey TA (1979) Functional organization in mouse barrel cortex. Brain Res 165:327-332.
67. Smith JM, Bradley DP, James MF, Huang CL (2006) Physiological studies of cortical spreading depression. Biol Rev Camb Philos Soc 81:457-481.
68. Somjen GG (2001) Mechanisms of spreading depression and hypoxic spreading depression-like depolarization. Physiol Rev 81:1065-1096.
69. Sosnik R, Haidarliu S, Ahissar E (2001) Temporal frequency of whisker movement. I. Representations in brain stem and thalamus. J Neuro-physiol 86:339-353.
70. Spacek J, Lieberman AR (1974) Ultrastructure and three-dimensional organization of synaptic glomeruli in rat somatosensory thalamus. J Anat 117:487-516.
71. Strong AJ, Fabricius M, Boutelle MG, Hibbins SJ, Hopwood SE, Jones R, Parkin MC, Lauritzen M (2002) Spreading and synchronous depressions of cortical activity in acutely injured human brain. Stroke 33:2738 -2743.
72. Takano T, Tian GF, Peng W, Lou N, Lovatt D, Hansen AJ, Kasischke KA, Nedergaard M (2007) Cortical spreading depression causes and coincides with tissue hypoxia. Nat Neurosci 10:754-762.
73. Takatsuru Y, Fukumoto D, Yoshitomo M, Nemoto T, Tsukada H, Nabekura J (2009) Neuronal circuit remodeling in the contralateral cortical hemisphere during functional recovery from cerebral infarction. J Neurosci 29:10081-10086.
74. Topolnik L, Steriade M, Timofeev I (2003) Hyperexcitability of intact neurons underlies acute development of trauma-related electrographic seizures in cats in vivo. Eur J Neurosci 18:486-496.
75. Urbain N, Deschênes M (2007) A new thalamic pathway of vibrissal information modulated by the motor cortex. J Neurosci 27:12407-12412.
76. Voronin LL, Cherubini E (2003) "Presynaptic silence" may be golden. Neu-ropharmacology 45:439-449.
77. Voronin LL, Cherubini E (2004) 'Deaf, mute and whispering' silent synapses: their role in synaptic plasticity. J Physiol 557:3-12.
78. Wang JH (2003) Short-term cerebral ischemia causes the dysfunction of interneurons and more excitation of pyramidal neurons in rats. Brain Res Bull 60:53-58.
79. Watanabe S, Hoffman JR, Craik RL, Hand PJ, Croul SE, Reivich M, Green-berg JH (2001) A new model of localized ischemia in rat somatosensory cortex produced by cortical compression. Stroke 32:2615-2623.
80. Webber RM, Stanley GB (2004) Nonlinear encoding of tactile patterns in the barrel cortex. J Neurophysiol 91:2010-2022.
81. Welch KM (2005) Brain hyperexcitability: the basis for antiepileptic drugs in migraine prevention. Headache 45 [Suppl 1]:S25-S32.
82. Welker C (1976) Receptive fields of barrels in the somatosensory neocortex of the rat. J Comp Neurol 166:173-189.
83. Woolsey TA, Van der Loos H (1970) The structural organization of layer IV in the somatosensory region (SI) of mouse cerebral cortex. The description of a cortical field composed of discrete cytoarchitectonic units. Brain Res 17:205-242.
84. Yang H, Zhang X, Chopp M, Jiang F, Schallert T (2006a) Local fluorouracil chemotherapy interferes with neural and behavioral recovery after brain tumor-like mass compression. Behav Brain Res 172:80-89.
85. Yang H, Chopp M, Jiang F, Zhang X, Schallert T (2006b) Interruption of functional recovery by the NMDA glutamate antagonist MK801 after compression of the sensorimotor cortex: implications for treatment of tumors or other mass-related brain injuries. Exp Neurol 200:262-266.
86. Yang L, Benardo LS, Valsamis H, Ling DS (2007) Acute injury to superficial cortex leads to a decrease in synaptic inhibition and increase in excitation in neocortical layer V pyramidal cells. J Neurophysiol 97:178-187.
87. Yang L, Afroz S, Michelson HB, Goodman JH, Valsamis HA, Ling DS (2010) Spontaneous epileptiform activity in rat neocortex after controlled cortical impact injury. J Neurotrauma 27:1541-1548.
88. Yu Z, Elkin BS, Morrison B (2009) Quantification of functional alterations after in vitro traumatic brain injury. Conf Proc IEEE Eng Med Biol Soc 2009:1135-1138.
89. Zhao X, Grotta J, Gonzales N, Aronowski J (2009) Hematoma resolution as a therapeutic target: the role of microglia/macrophages. Stroke 40: S92-S94.