Age dependence of excitatory-inhibitory balance following stroke

Neurobiology of Aging

Volumn 33, Issue 7, 2012, Pages 1356-1363

  Schmidt, Silvio ^a   Bruehl, Claus ^a,b   Frahm, Christiane ^a   Redecker, Christoph ^a   Witte, Otto W ^a  

^a FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

Aging; Brain excitability; GABAA receptor; Photothrombosis; Stroke

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR ALPHA1; 4 AMINOBUTYRIC ACID A RECEPTOR ALPHA2; 4 AMINOBUTYRIC ACID A RECEPTOR ALPHA3; 4 AMINOBUTYRIC ACID A RECEPTOR ALPHA5; 4 AMINOBUTYRIC ACID A RECEPTOR GAMMA2;

AGE DISTRIBUTION; AGED; AGING; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX LESION; BRAIN ELECTROPHYSIOLOGY; BRAIN REGION; BRAIN SLICE; CONTROLLED STUDY; EVOKED CORTICAL RESPONSE; EXCITATORY INHIBITORY BALANCE; MALE; NEUROPATHOLOGY; NONHUMAN; OCCLUSIVE CEREBROVASCULAR DISEASE; PAIRED PULSE INHIBITION; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; STIMULUS RESPONSE; STROKE; TISSUE DISTRIBUTION; WHITE MATTER;

AGING; ANIMALS; BRAIN; EXCITATORY POSTSYNAPTIC POTENTIALS; MALE; NEURAL INHIBITION; RATS; RATS, WISTAR; RECEPTORS, GABA-A; STROKE;

EID: 84861186802     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2010.11.019     Document Type: Article

References (63)

1. Alaverdashvili M., Whishaw I.Q. Compensation aids skilled reaching in aging and in recovery from forelimb motor cortex stroke in the rat. Neuroscience 2010, 167:21-30.
2. Artola A., Brocher S., Singer W. Different voltage-dependent thresholds for inducing long-term depression and long-term potentiation in slices of rat visual cortex. Nature 1990, 347:69-72.
3. Artola A., Singer W. Long-term potentiation and NMDA receptors in rat visual cortex. Nature 1987, 330:649-652.
4. Atack J.R., Bayley P.J., Seabrook G.R., Wafford K.A., McKernan R.M., Dawson G.R. L-655,708 enhances cognition in rats but is not proconvulsant at a dose selective for alpha5-containing GABAA receptors. Neuropharmacology 2006, 51:1023-1029.
5. Badan I., Buchhold B., Hamm A., Gratz M., Walker L.C., Platt D., Kessler C., Popa-Wagner A. Accelerated glial reactivity to stroke in aged rats correlates with reduced functional recovery. J. Cereb. Blood Flow Metab 2003, 23:845-854.
6. Ballard T.M., Knoflach F., Prinssen E., Borroni E., Vivian J.A., Basile J., Gasser R., Moreau J.L., Wettstein J.G., Buettelmann B., Knust H., Thomas A.W., Trube G., Hernandez M.C. RO 4938581, a novel cognitive enhancer acting at GABAA alpha5 subunit-containing receptors. Psychopharmacology (Berl.) 2009, 202:207-223.
7. Bastings E.P., Greenberg J.P., Good D.C. Hand motor recovery after stroke: a transcranial magnetic stimulation mapping study of motor output areas and their relation to functional status. Neurorehabil. Neural Repair 2002, 16:275-282.
8. Bohlhalter S., Weinmann O., Mohler H., Fritschy J.M. Laminar compartmentalization of GABAA-receptor subtypes in the spinal cord: an immunohistochemical study. J. Neurosci 1996, 16:283-297.
9. Brown A.W., Marlowe K.J., Bjelke B. Age effect on motor recovery in a post-acute animal stroke model. Neurobiol. Aging 2003, 24:607-614.
10. Brown C.E., Aminoltejari K., Erb H., Winship I.R., Murphy T.H. In vivo voltage-sensitive dye imaging in adult mice reveals that somatosensory maps lost to stroke are replaced over weeks by new structural and functional circuits with prolonged modes of activation within both the peri-infarct zone and distant sites. J. Neurosci 2009, 29:1719-1734.
11. Buchhold B., Mogoanta L., Suofu Y., Hamm A., Walker L., Kessler C., Popa-Wagner A. Environmental enrichment improves functional and neuropathological indices following stroke in young and aged rats. Restor. Neurol. Neurosci 2007, 25:467-484.
12. Caraiscos V.B., Elliott E.M., You-Ten K.E., Cheng V.Y., Belelli D., Newell J.G., Jackson M.F., Lambert J.J., Rosahl T.W., Wafford K.A., MacDonald J.F., Orser B.A. Tonic inhibition in mouse hippocampal CA1 pyramidal neurons is mediated by alpha5 subunit-containing gamma-aminobutyric acid type A receptors. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:3662-3667.
13. Castro-Alamancos M.A., Donoghue J.P., Connors B.W. Different forms of synaptic plasticity in somatosensory and motor areas of the neocortex. J. Neurosci 1995, 15:5324-5333.
14. Chambers M.S., Atack J.R., Broughton H.B., Collinson N., Cook S., Dawson G.R., Hobbs S.C., Marshall G., Maubach K.A., Pillai G.V., Reeve A.J., MacLeod A.M. Identification of a novel, selective GABA(A) alpha5 receptor inverse agonist which enhances cognition. J. Med. Chem 2003, 46:2227-2240.
15. Collinson N., Kuenzi F.M., Jarolimek W., Maubach K.A., Cothliff R., Sur C., Smith A., Otu F.M., Howell O., Atack J.R., McKernan R.M., Seabrook G.R., Dawson G.R., Whiting P.J., Rosahl T.W. Enhanced learning and memory and altered GABAergic synaptic transmission in mice lacking the alpha 5 subunit of the GABAA receptor. J. Neurosci 2002, 22:5572-5580.
16. Cramer S.C., Chopp M. Recovery recapitulates ontogeny. Trends Neurosci 2000, 23:265-271.
17. Cramer S.C., Nelles G., Benson R.R., Kaplan J.D., Parker R.A., Kwong K.K., Kennedy D.N., Finklestein S.P., Rosen B.R. A functional MRI study of subjects recovered from hemiparetic stroke. Stroke 1997, 28:2518-2527.
18. Davis G.W. Homeostatic control of neural activity: from phenomenology to molecular design. Annu. Rev. Neurosci 2006, 29:307-323.
19. Derdikman D., Hildesheim R., Ahissar E., Arieli A., Grinvald A. Imaging spatiotemporal dynamics of surround inhibition in the barrels somatosensory cortex. J. Neurosci 2003, 23:3100-3105.
20. Dijkhuizen R.M., Ren J., Mandeville J.B., Wu O., Ozdag F.M., Moskowitz M.A., Rosen B.R., Finklestein S.P. Functional magnetic resonance imaging of reorganization in rat brain after stroke. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:12766-12771.
21. Dykes R.W. Mechanisms controlling neuronal plasticity in somatosensory cortex. Can. J. Physiol. Pharmacol 1997, 75:535-545.
22. Farrant M., Nusser Z. Variations on an inhibitory theme: phasic and tonic activation of GABA(A) receptors. Nat. Rev. Neurosci 2005, 6:215-229.
23. Feldman D.E. Synaptic mechanisms for plasticity in neocortex. Annu. Rev. Neurosci 2009, 32:33-55.
24. Foeller E., Celikel T., Feldman D.E. Inhibitory sharpening of receptive fields contributes to whisker map plasticity in rat somatosensory cortex. J. Neurophysiol 2005, 94:4387-4400.
25. Friel K.M., Heddings A.A., Nudo R.J. Effects of postlesion experience on behavioral recovery and neurophysiologic reorganization after cortical injury in primates. Neurorehabil. Neural Repair 2000, 14:187-198.
26. Fritschy J.M., Mohler H. GABAA-receptor heterogeneity in the adult rat brain: differential regional and cellular distribution of seven major subunits. J. Comp. Neurol 1995, 359:154-194.
27. Fritschy J.M., Paysan J., Enna A., Mohler H. Switch in the expression of rat GABAA-receptor subtypes during postnatal development: an immunohistochemical study. J. Neurosci 1994, 14:5302-5324.
28. Fritschy J.M., Schweizer C., Brunig I., Luscher B. Pre- and post-synaptic mechanisms regulating the clustering of type A gamma-aminobutyric acid receptors (GABAA receptors). Biochem. Soc. Trans 2003, 31:889-892.
29. Fritschy J.M., Weinmann O., Wenzel A., Benke D. Synapse-specific localization of NMDA and GABA(A) receptor subunits revealed by antigen-retrieval immunohistochemistry. J. Comp. Neurol 1998, 390:194-210.
30. Hagemann G., Redecker C., Neumann-Haefelin T., Freund H.J., Witte O.W. Increased long-term potentiation in the surround of experimentally induced focal cortical infarction. Ann. Neurol 1998, 44:255-258.
31. Hensch T.K. Critical period regulation. Annu. Rev. Neurosci 2004, 27:549-579.
32. Hensch T.K. Critical period plasticity in local cortical circuits. Nat. Rev. Neurosci 2005, 6:877-888.
33. Hensch T.K., Stryker M.P. Columnar architecture sculpted by GABA circuits in developing cat visual cortex. Science 2004, 303:1678-1681.
34. Hess G., Donoghue J.P. Long-term potentiation of horizontal connections provides a mechanism to reorganize cortical motor maps. J. Neurophysiol 1994, 71:2543-2547.
35. Jablonka J.A., Burnat K., Witte O.W., Kossut M. Remapping of the somatosensory cortex after a photothrombotic stroke: dynamics of the compensatory reorganization. Neuroscience 2010, 165:90-100.
36. Jaillard A., Martin C.D., Garambois K., Lebas J.F., Hommel M. Vicarious function within the human primary motor cortex?. A longitudinal fMRI stroke study. Brain 2005, 128:1122-1138.
37. Kirkwood A., Bear M.F. Hebbian synapses in visual cortex. J. Neurosci 1994, 14:1634-1645.
38. Liepert J., Uhde I., Graf S., Leidner O., Weiller C. Motor cortex plasticity during forced-use therapy in stroke patients: a preliminary study. J. Neurol 2001, 248:315-321.
39. Markus T.M., Tsai S.Y., Bollnow M.R., Farrer R.G., O'Brien T.E., Kindler-Baumann D.R., Rausch M., Rudin M., Wiessner C., Mir A.K., Schwab M.E., Kartje G.L. Recovery and brain reorganization after stroke in adult and aged rats. Ann. Neurol 2005, 58:950-953.
40. Martin L.J., Zurek A.A., MacDonald J.F., Roder J.C., Jackson M.F., Orser B.A. Alpha5GABAA receptor activity sets the threshold for long-term potentiation and constrains hippocampus-dependent memory. J. Neurosci 2010, 30:5269-5282.
41. McCutcheon J.E., Marinelli M. Age matters. Eur. J. Neurosci 2009, 29:997-1014.
42. Neumann-Haefelin T., Witte O.W. Periinfarct and remote excitability changes after transient middle cerebral artery occlusion. J. Cereb. Blood Flow Metab 2000, 20:45-52.
43. Nudo R.J., Wise B.M., Sifuentes F., Milliken G.W. Neural substrates for the effects of rehabilitative training on motor recovery after ischemic infarct. Science 1996, 272:1791-1794.
44. Pizzorusso T., Medini P., Berardi N., Chierzi S., Fawcett J.W., Maffei L. Reactivation of ocular dominance plasticity in the adult visual cortex. Science 2002, 298:1248-1251.
45. Porter J.T., Johnson C.K., Agmon A. Diverse types of interneurons generate thalamus-evoked feedforward inhibition in the mouse barrel cortex. J. Neurosci 2001, 21:2699-2710.
46. Redecker C., Luhmann H.J., Hagemann G., Fritschy J.M., Witte O.W. Differential downregulation of GABAA receptor subunits in widespread brain regions in the freeze-lesion model of focal cortical malformations. J. Neurosci 2000, 20:5045-5053.
47. Redecker C., Wang W., Fritschy J.M., Witte O.W. Widespread and long-lasting alterations in GABA(A)-receptor subtypes after focal cortical infarcts in rats: mediation by NMDA-dependent processes. J. Cereb. Blood Flow Metab 2002, 22:1463-1475.
48. Reinecke S., Dinse H.R., Reinke H., Witte O.W. Induction of bilateral plasticity in sensory cortical maps by small unilateral cortical infarcts in rats. Eur. J. Neurosci 2003, 17:623-627.
49. Rossini P.M., Calautti C., Pauri F., Baron J.C. Post-stroke plastic reorganisation in the adult brain. Lancet Neurol 2003, 2:493-502.
50. Rozas C., Frank H., Heynen A.J., Morales B., Bear M.F., Kirkwood A. Developmental inhibitory gate controls the relay of activity to the superficial layers of the visual cortex. J. Neurosci 2001, 21:6791-6801.
51. Saghatelyan A.K., Dityatev A., Schmidt S., Schuster T., Bartsch U., Schachner M. Reduced perisomatic inhibition, increased excitatory transmission, and impaired long-term potentiation in mice deficient for the extracellular matrix glycoprotein tenascin-R. Mol. Cell. Neurosci 2001, 17:226-240.
52. Sawaki L., Butler A.J., Xiaoyan L., Wassenaar P.A., Mohammad Y.M., Blanton S., Sathian K., Nichols-Larsen D.S., Wolf S.L., Good D.C., Wittenberg G.F. Constraint-induced movement therapy results in increased motor map area in subjects 3 to 9 months after stroke. Neurorehabil. Neural Repair 2008, 22:505-513.
53. Schiene K., Bruehl C., Zilles K., Qu M., Hagemann G., Kraemer M., Witte O.W. Neuronal hyperexcitability and reduction of GABAA-receptor expression in the surround of cerebral photothrombosis. J. Cereb. Blood Flow Metab 1996, 16:906-914.
54. Schmidt S., Redecker C., Bruehl C., Witte O.W. Age-related decline of functional inhibition in rat cortex. Neurobiol. Aging 2010, 31:504-511.
55. Recommendations for standards regarding preclinical neuroprotective and restorative drug development. Stroke 1999, 30:2752-2758. STAIR.
56. Turrigiano G.G., Nelson S.B. Homeostatic plasticity in the developing nervous system. Nat. Rev. Neurosci 2004, 5:97-107.
57. Witte O.W., Stoll G. Delayed and remote effects of focal cortical infarctions: secondary damage and reactive plasticity. Adv. Neurol 1997, 73:207-227.
58. Yu Z.Y., Wang W., Fritschy J.M., Witte O.W., Redecker C. Changes in neocortical and hippocampal GABAA receptor subunit distribution during brain maturation and aging. Brain Res. 2006, 1099:73-81.
59. Zepeda A., Sengpiel F., Guagnelli M.A., Vaca L., Arias C. Functional reorganization of visual cortex maps after ischemic lesions is accompanied by changes in expression of cytoskeletal proteins and NMDA and GABA(A) receptor subunits. J. Neurosci 2004, 24:1812-1821.
60. Zhang L., Zhang R.L., Wang Y., Zhang C., Zhang Z.G., Meng H., Chopp M. Functional recovery in aged and young rats after embolic stroke: treatment with a phosphodiesterase type 5 inhibitor. Stroke 2005, 36:847-852.
61. Zheng W., Knudsen E.I. Gabaergic inhibition antagonizes adaptive adjustment of the owl's auditory space map during the initial phase of plasticity. J. Neurosci 2001, 21:4356-4365.
62. Ziemann U., Hallett M., Cohen L.G. Mechanisms of deafferentation-induced plasticity in human motor cortex. J. Neurosci 1998, 18:7000-7007.
63. Zilles K. The Cortex of the Rat, a Stereotaxic Atlas 1985, Springer-Verlag, Heidelberg.