Astrocyte-mediated hepatocyte growth factor/scatter factor supplementation restores GABAergic interneurons and corrects reversal learning deficits in mice

Journal of Neuroscience

Volumn 30, Issue 8, 2010, Pages 2918-2923

  Bissonette, Gregory B ^a   Bae, Mihyun H ^a   Suresh, Tejas ^a   Jaffe, David E ^a   Powell, Elizabeth M ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; GROWTH FACTOR; PARVALBUMIN; SCATTER FACTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BEHAVIOR; CONTROLLED STUDY; INTERNEURON; LEARNING; LEARNING DISORDER; MALE; MOUSE; NONHUMAN; ONTOGENY; ORBITAL CORTEX; PRIORITY JOURNAL; SUPPLEMENTATION;

ANIMALS; ASTROCYTES; BIOLOGICAL MARKERS; CORPUS STRIATUM; GAMMA-AMINOBUTYRIC ACID; HEPATOCYTE GROWTH FACTOR; IMMUNOHISTOCHEMISTRY; INTERNEURONS; LEARNING DISORDERS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; NERVOUS SYSTEM MALFORMATIONS; NEURAL PATHWAYS; NEUROPSYCHOLOGICAL TESTS; PARVALBUMINS; PREFRONTAL CORTEX; PROSENCEPHALON; TREATMENT OUTCOME;

EID: 77649109147     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5268-09.2010     Document Type: Article

References (47)

1. Achim CL, Katyal S, Wiley CA, Shiratori M, Wang G, Oshika E, Petersen BE, Li JM, Michalopoulos GK (1997) Expression of HGF and cMet in the developing and adult brain. Brain Res Dev Brain Res 102:299-303.
2. Anderson SA, Qiu M, Bulfone A, Eisenstat DD, Meneses J, Pedersen R, Rubenstein JL (1997) Mutations of the homeobox genes Dlx-1 and Dlx-2 disrupt the striatal subventricular zone and differentiation of late born striatal neurons. Neuron 19:27-37.
3. Anderson SA, Marín O, Horn C, Jennings K, Rubenstein JL (2001) Distinct cortical migrations from the medial and lateral ganglionic eminences. Development 128:353-363.
4. Avoli M, Bernasconi A, Mattia D, Olivier A, Hwa GG (1999) Epileptiform discharges in the human dysplastic neocortex: in vitro physiology and pharmacology. Ann Neurol 46:816-826.
5. Bae M, Harmon MCJ, Mars WM, Michalopoulos GK, Achim C, Powell EM (2005) Critical roles for uPAR and HGF/SF in brain development and epilepsy. Thromb Haemo 93:A2.
6. Bae MH, Bissonette GB, Mars WM, Michalopoulos GK, Achim C, Depireux DA, Powell EM (2010) Hepatocyte growth factor (HGF) modulates GABAergic inhibition and seizure susceptibility. Exp Neurol 221: 129-135.
7. Baulac S, Huberfeld G, Gourfinkel-An I, Mitropoulou G, Beranger A, Prud'homme JF, Baulac M, Brice A, Bruzzone R, LeGuern E (2001) First genetic evidence of GABA(A) receptor dysfunction in epilepsy: a mutation in the gamma2-subunit gene. Nat Genet 28:46-48.
8. Beasley CL, Reynolds GP (1997) Parvalbumin-immunoreactive neurons are reduced in the prefrontal cortex of schizophrenics. Schizophr Res 24:349-355.
9. Bellebaum C, Koch B, Schwarz M, Daum I (2008) Focal basal ganglia lesions are associated with impairments in reward-based reversal learning. Brain 131:829-841.
10. Benes FM, McSparren J, Bird ED, SanGiovanni JP, Vincent SL (1991) Deficits in small interneurons in prefrontal and cingulate cortices of schizophrenic and schizoaffective patients. Arch Gen Psychiatry 48:996-1001.
11. Berghuis P, Dobszay MB, Sousa KM, Schulte G, Mager PP, Härtig W, Görcs TJ, Zilberter Y, Ernfors P, Harkany T (2004) Brain-derived neurotrophic factor controls functional differentiation and microcircuit formation of selectively isolated fast-spiking GABAergic interneurons. Eur J Neurosci 20:1290-1306.
12. Bissonette GB, Martins GJ, Franz TM, Harper ES, Schoenbaum G, Powell EM (2008) Double dissociation of the effects of medial and orbital prefrontal cortical lesions on attentional and affective shifts in mice. J Neurosci 28:11124-11130.
13. Brigman JL, Bussey TJ, Saksida LM, Rothblat LA (2005) Discrimination of multidimensional visual stimuli by mice: intra- and extradimensional shifts. Behav Neurosci 119:839-842.
14. Clarke HF, Robbins TW, Roberts AC (2008) Lesions of the medial striatum in monkeys produce perseverative impairments during reversal learning similar to those produced by lesions of the orbitofrontal cortex. J Neurosci 28:10972-10982.
15. Cobos I, Calcagnotto ME, Vilaythong AJ, Thwin MT, Noebels JL, Baraban SC, Rubenstein JL (2005) Mice lacking Dlx1 show subtype-specific loss of interneurons, reduced inhibition and epilepsy. Nat Neurosci 8:1059-1068.
16. Colacicco G, Welzl H, Lipp HP,WürbelH (2002) Attentional set-shifting in mice: modification of a rat paradigm, and evidence for strain-dependent variation. Behav Brain Res 132:95-102.
17. Cools R, Clark L, Owen AM, RobbinsTW (2002) Defining the neural mechanisms of probabilistic reversal learning using event-related functional magnetic resonance imaging. J Neurosci 22:4563-4567.
18. Dewerchin M, Nuffelen AV, Wallays G, Bouché A, Moons L, Carmeliet P, Mulligan RC, Collen D (1996) Generation and characterization of urokinase receptor-deficient mice. J Clin Invest 97:870-878.
19. Dias R, Robbins TW, Roberts AC (1996a) Primate analogue of the Wisconsin Card Sorting Test: effects of excitotoxic lesions of the prefrontal cortex in the marmoset. Behav Neurosci 110:872-886.
20. Dias R, Robbins TW, Roberts AC (1996b) Dissociation in prefrontal cortex of affective and attentional shifts. Nature 380:69-72.
21. Eagleson KL, Bonnin A, Levitt P (2005) Region- and age-specific deficits in gamma-aminobutyric acidergic neuron development in the telencephalon of the uPAR(-/-) mouse. J Comp Neurol 489:449-466.
22. Ferrer I, Oliver B, Russi A, Casas R, Rivera R (1994) Parvalbumin and calbindin-D28k immunocytochemistry in human neocortical epileptic foci. J Neurol Sci 123:18-25.
23. Galloway EM, Woo NH, Lu B (2008) Persistent neural activity in the prefrontal cortex: a mechanism by which BDNF regulates working memory? Prog Brain Res 169:251-266.
24. Hashimoto T, Arion D, Unger T, Maldonado-Avilés JG, Morris HM, Volk DW, Mirnics K, Lewis DA (2008) Alterations in GABA-related transcriptome in the dorsolateral prefrontal cortex of subjects with schizophrenia. Mol Psychiatry 13:147-161.
25. Howard CV, Reed MG (1998) Unbiased stereology, Ed 1. New York: Garland Science/BIOS Scientific Publishers.
26. Kim J, RagozzinoME (2005) The involvement of the orbitofrontal cortex in learning under changing task contingencies. Neurobiol Learn Mem 83:125-133.
27. Letinic K, Zoncu R, Rakic P (2002) Origin of GABAergic neurons in the human neocortex. Nature 417:645-649.
28. Lewis DA, Hashimoto T, Volk DW (2005) Cortical inhibitory neurons and schizophrenia. Nat Rev Neurosci 6:312-324.
29. Marin O, Anderson SA, Rubenstein JL (2000) Origin and molecular specification of striatal interneurons. J Neurosci 20:6063-6076.
30. Martins GJ, Plachez C, Powell EM (2007) Loss of embryonic MET signaling alters profiles of hippocampal interneurons. Dev Neurosci 29:143-158.
31. McAlonan K, Brown VJ (2003) Orbital prefrontal cortex mediates reversal learning and not attentional set shifting in the rat. Behav Brain Res 146:97-103.
32. Nery S, Fishell G, Corbin JG (2002) The caudal ganglionic eminence is a source of distinct cortical and subcortical cell populations. Nat Neurosci 5:1279-1287.
33. O'Doherty J, Kringelbach ML, Rolls ET, Hornak J, Andrews C (2001) Abstract reward and punishment representations in the human orbitofrontal cortex. Nat Neurosci 4:95-102.
34. Paxinos G, Franklin KBJ (2001) The mouse brain in stereotaxic coordinates, Ed 2. San Diego: Academic.
35. Porter BE, Brooks-Kayal A, Golden JA (2002) Disorders of cortical development and epilepsy. Arch Neurol 59:361-365.
36. Powell EM, Mars WM, Levitt P (2001) Hepatocyte growth factor/scatter factor is a motogen for interneurons migrating from the ventral to dorsal telencephalon. Neuron 30:79-89.
37. Powell EM, Campbell DB, Stanwood GD, Davis C, Noebels JL, Levitt P (2003) Genetic disruption of cortical interneuron development causes region- and GABA cell type-specific deficits, epilepsy, and behavioral dysfunction. J Neurosci 23:622-631.
38. Ragozzino ME (2007) The contribution of the medial prefrontal cortex, orbitofrontal cortex, and dorsomedial striatum to behavioral flexibility. Ann N Y Acad Sci 1121:355-375.
39. Schoenbaum G, Chiba AA, Gallagher M (1998) Orbitofrontal cortex and basolateral amygdala encode expected outcomes during learning. Nat Neurosci 1:155-159.
40. Schoenbaum G, Setlow B, Nugent SL, Saddoris MP, Gallagher M (2003) Lesions of orbitofrontal cortex and basolateral amygdala complex disrupt acquisition of odor-guided discriminations and reversals. Learn Mem 10:129-140.
41. Seymour B, Daw N, Dayan P, Singer T, Dolan R (2007) Differential encoding of losses and gains in the human striatum. J Neurosci 27:4826-4831.
42. Stork O, Ji FY, Kaneko K, Stork S, Yoshinobu Y, Moriya T, Shibata S, Obata K (2000) Postnatal development of a GABA deficit and disturbance of neural functions in mice lacking GAD65. Brain Res 865:45-58.
43. Tait DS, Brown VJ (2008) Lesions of the basal forebrain impair reversal learning but not shifting of attentional set in rats. Behav Brain Res 187:100-108.
44. Tamminga C, Hashimoto T, Volk DW, Lewis DA (2004) GABA neurons in the human prefrontal cortex. Am J Psychiatry 161:1764.
45. Thewke DP, Seeds NW (1999) The expression of mRNAs for hepatocyte growth factor/scatter factor, its receptor c-met, and one of its activators tissue-type plasminogen activator show a systematic relationship in the developing and adult cerebral cortex and hippocampus. Brain Res 821:356-367.
46. West MJ (1999) Stereological methods for estimating the total number of neurons and synapses: issues of precision and bias. Trends Neurosci 22:51-61.
47. Wonders CP, Anderson SA (2006) The origin and specification of cortical interneurons. Nat Rev Neurosci 7:687-696.