Regulation of cortical interneurons by neurotrophins: From development to cognitive disorders

Neuroscientist

Volumn 12, Issue 1, 2006, Pages 43-56

  Woo, Newton H ^a   Lu, Bai ^a,b  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

Author keywords

Axo axonic; Basket cells; BDNF; Chandelier cells; Epilepsy; GABA; Parvalbumin; Schizophrenia

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; CHLORIDE ION; NEUROTROPHIN; PARVALBUMIN;

BASKET CELL; BRAIN CORTEX; BRAIN DEVELOPMENT; CELL FUNCTION; CELL MIGRATION; CELL TYPE; CENTRAL NERVOUS SYSTEM DISEASE; CHANDELIER CELL; COGNITION; COGNITIVE DEFECT; EPILEPSY; HOMEOSTASIS; HUMAN; INTERNEURON; MAMMAL; NERVE CELL; NERVE CELL DIFFERENTIATION; NERVE FIBER; NEUROTRANSMISSION; NONHUMAN; PATHOLOGY; PRIORITY JOURNAL; PROTEIN FUNCTION; PYRAMIDAL NERVE CELL; REVIEW; SCHIZOPHRENIA; SYNAPSE; SYNAPTOGENESIS;

ANIMALS; CENTRAL NERVOUS SYSTEM DISEASES; CEREBRAL CORTEX; COGNITION DISORDERS; GAMMA-AMINOBUTYRIC ACID; HUMANS; INTERNEURONS; NERVE GROWTH FACTORS; NERVE NET;

EID: 31044447651     PISSN: 10738584     EISSN: 10894098     Source Type: Journal    
DOI: 10.1177/1073858405284360     Document Type: Review

References (107)

1. Aguado F, Carmona MA, Pozas E, Aguilo A, Martinez-Guijarro FJ, Alcantara S, and others. 2003. BDNF regulates spontaneous correlated activity at early developmental stages by increasing synaptogenesis and expression of the K+/Cl- co-transporter KCC2. Development 130:1267-80.
2. Akbarian S, Kim JJ, Potkin SG, Hagman JO, Tafazzoli A, Bunney WE Jr, and others. 1995. Gene expression for glutamic acid decarboxylase is reduced without loss of neurons in prefrontal cortex of schizophrenics. Arch Gen Psychiatry 52:258-66.
3. Altar CA, Boylan CB, Fritsche M, Jackson C, Hyman C, Lindsay RM. 1994. The neurotrophins NT-4/5 and BDNF augment serotonin, dopamine, and GABAergic systems during behaviorally effective infusions to the substantia nigra. Exp Neurol 130:31-40.
4. Altar CA, Cai N, Bliven T, Juhasz M, Conner JM, Acheson AL, and others. 1997. Anterograde transport of brain-derived neurotrophic factor and its role in the brain. Nature 389:856-60.
5. Arellano JI, Munoz A, Ballesteros-Yanez I, Sola RG, DeFelipe J. 2004. Histopathology and reorganization of chandelier cells in the human epileptic sclerotic hippocampus. Brain 127:45-64.
6. Azouz R, Alroy G, Yaari Y. 1997. Modulation of endogenous firing patterns by osmolarity in rat hippocampal neurones. J Physiol 502:175-87.
7. Baldelli P, Hernandez-Guijo JM, Carabelli V, Carbone E. 2005. Brain-derived neurotrophic factor enhances GABA release probability and nonuniform distribution of N- and P/Q-type channels on release sites of hippocampal inhibitory synapses. J Neurosci 25:3358-68.
8. Beasley CL, Reynolds GP. 1997. Parvalbumin-immunoreactive neurons are reduced in the prefrontal cortex of schizophrenics. Schizophr Res 24:349-55.
9. Ben-Ari Y. 2001. Developing networks play a similar melody. Trends Neurosci 24:353-60.
10. Ben-Ari Y, Khalilov I, Represa A, Gozlan H. 2004. Interneurons set the tune of developing networks. Trends Neurosci 27:422-7.
11. Ben-Ari Y, Khazipov R, Leinekugel X, Gaillard O, Gaiarsa JL. 1997. GABAA, NMDA and AMPA receptors: a developmentally regulated 'menage a trois'. Trends Neurosci 20:523-9.
12. Berghuis P, Dobszay MB, Sousa KM, Schulte G, Mager PP, Hartig W, and others. 2004. Brain-derived neurotrophic factor controls functional differentiation and microcircuit formation of selectively isolated fast-spiking GABAergic interneurons. Eur J Neurosci 20:1290-306.
13. Binder DK, Routbort MJ, McNamara JO. 1999. Immunohistochemical evidence of seizure-induced activation of trk receptors in the mossy fiber pathway of adult rat hippocampus. J Neurosci 19:4616-26.
14. Blatow M, Rozov A, Katona I, Hormuzdi SG, Meyer AH, Whittington MA, and others. 2003. A novel network of multipolar bursting interneurons generates theta frequency oscillations in neocortex. Neuron 38:805-17.
15. Brunig I, Penschuck S, Berninger B, Benson J, Fritschy JM. 2001. BDNF reduces miniature inhibitory postsynaptic currents by rapid downregulation of GABA(A) receptor surface expression. Eur J Neurosci 13:1320-8.
16. Buzsaki G, Draguhn A. 2004. Neuronal oscillations in cortical networks. Science 304:1926-9.
17. Cellerino A, Maffei L, Domenici L. 1996. The distribution of brain-derived neurotrophic factor and its receptor trkB in parvalbumin- containing neurons of the rat visual cortex. Eur J Neurosci 8:1190-7.
18. Cepeda C, Starling AJ, Wu N, Nguyen OK, Uzgil B, Soda T, and others. 2004. Increased GABAergic function in mouse models of Huntington's disease: reversal by BDNF. J Neurosci Res 78:855-67.
19. Chao MV. 2003. Neurotrophins and their receptors: a convergence point for many signalling pathways. Nat Rev Neurosci 4:299-309.
20. Cheng Q, Yeh HH. 2003. Brain-derived neurotrophic factor attenuates mouse cerebellar granule cell GABA(A) receptor-mediated responses via postsynaptic mechanisms. J Physiol 548:711-21.
21. Cobb SR, Buhl EH, Halasy K, Paulsen O, Somogyi P. 1995. Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons. Nature 378:75-8.
22. Cobos I, Calcagnotto ME, Vilaythong AJ, Thwin MT, Noebels JL, Baraban SC, and others. 2005. Mice lacking Dlx1 show subtype-specific loss of interneurons, reduced inhibition and epilepsy. Nat Neurosci 8:1059-68.
23. Collin C, Vicario-Abejon C, Rubio ME, Wenthold RJ, McKay RD, Segal M. 2001. Neurotrophins act at presynaptic terminals to activate synapses among cultured hippocampal neurons. Eur J Neurosci 13:1273-82.
24. Croll SD, Suri C, Compton DL, Simmons MV, Yancopoulos GD, Lindsay RM, and others. 1999. Brain-derived neurotrophic factor transgenic mice exhibit passive avoidance deficits, increased seizure severity and in vitro hyperexcitability in the hippocampus and entorhinal cortex. Neuroscience 93:1491-506.
25. DeFelipe J. 1999. Chandelier cells and epilepsy. Brain 122(Pt 10):1807-22.
26. Elmariah SB, Crumling MA, Parsons TD, Balice-Gordon RJ. 2004. Postsynaptic TrkB-mediated signaling modulates excitatory and inhibitory neurotransmitter receptor clustering at hippocampal synapses. J Neurosci 24:2380-93.
27. Engel AK, Fries P, Singer W. 2001. Dynamic predictions: oscillations and synchrony in top-down processing. Nat Rev Neurosci 2:704-16.
28. Ernfors P, Bengzon J, Kokaia Z, Persson H, Lindvall O. 1991. Increased levels of messenger RNAs for neurotrophic factors in the brain during kindling epileptogenesis. Neuron 7:165-76.
29. Feller MB. 1999. Spontaneous correlated activity in developing neural circuits. Neuron 22:653-6.
30. Fisahn A, Pike FG, Buhl EH, Paulsen O. 1998. Cholinergic induction of network oscillations at 40 Hz in the hippocampus in vitro. Nature 394:186-9.
31. Frerking M, Malenka RC, Nicoll RA. 1998. Brain-derived neurotrophic factor (BDNF) modulates inhibitory, but not excitatory, transmission in the CA1 region of the hippocampus. J Neurophysiol 80:3383-6.
32. Freund TF. 2003. Interneuron diversity series: rhythm and mood in perisomatic inhibition. Trends Neurosci 26:489-95.
33. Galarreta M, Hestrin S. 1999. A network of fast-spiking cells in the neocortex connected by electrical synapses. Nature 402:72-5.
34. Gao XB, van den Pol AN. 1999. Neurotrophin-3 potentiates excitatory GABAergic synaptic transmission in cultured developing hypothalamic neurones of the rat. J Physiol 518(Pt 1):81-95.
35. Goldman-Rakic PS. 1995. Cellular basis of working memory. Neuron 14:477-85.
36. Gorba T, Wahle P. 1999. Expression of TrkB and TrkC but not BDNF mRNA in neurochemically identified interneurons in rat visual cortex in vivo and in organotypic cultures. Eur J Neurosci 11:1179-90.
37. Hashimoto T, Bergen SE, Nguyen QL, Xu B, Monteggia LM, Pierri JN, and others. 2005. Relationship of brain-derived neurotrophic factor and its receptor TrkB to altered inhibitory prefrontal circuitry in schizophrenia. J Neurosci 25:372-83.
38. Hashimoto T, Volk DW, Eggan SM, Mimics K, Pierri JN, Sun Z, and others. 2003. Gene expression deficits in a subclass of GABA neurons in the prefrontal cortex of subjects with schizophrenia. J Neurosci 23:6315-26.
39. He XP, Kotloski R, Nef S, Luikart BW, Parada LF, McNamara JO. 2004. Conditional deletion of TrkB but not BDNF prevents epileptogenesis in the kindling model. Neuron 43:31-42.
40. Hicks TP, Dykes RW. 1983. Receptive field size for certain neurons in primary somatosensory cortex is determined by GABA-mediated intracortical inhibition. Brain Res 274:160-4.
41. Howard MW, Rizzuto DS, Caplan JB, Madsen JR, Lisman J, Aschenbrenner-Scheibe R, and others. 2003. Gamma oscillations correlate with working memory load in humans. Cereb Cortex 13:1369-74.
42. Huang EJ, Reichardt LF. 2003. Trk receptors: roles in neuronal signal transduction. Annu Rev Biochem 72:609-42. Epub 2003 Mar 2027.
43. Huang ZJ, Kirkwood A, Pizzorusso T, Porciatti V, Morales B, Bear MF, and others. 1999. BDNF regulates the maturation of inhibition and the critical period of plasticity in mouse visual cortex. Cell 98:739-55.
44. Hyman C, Juhasz M, Jackson C, Wright P, Ip N, Lindsay RM. 1994. Overlapping and distinct actions of the neurotrophins BDNF, NT-3, and NT-4/5 on cultured dopaminergic and GABAergic neurons of the ventral mesencephalon. J Neurosci 14:335-47.
45. Iritani S, Niizato K, Nawa H, Ikeda K, Emson PC. 2003. Imraunohistochemical study of brain-derived neurotrophic factor and its receptor, TrkB, in the hippocampal formation of schizophrenic brains. Prog Neuropsychopharmacol Biol Psychiatry 27:801-7.
46. Isackson PJ, Huntsman MM, Murray KD, Gall CM. 1991. BDNF mRNA expression is increased in adult rat forebrain after limbic seizures: temporal patterns of induction distinct from NGF. Neuron 6:937-48.
47. Jin X, Hu H, Mathers PH, Agmon A. 2003. Brain-derived neurotrophic factor mediates activity-dependent dendritic growth in nonpyramidal neocortical interneurons in developing organotypic cultures. J Neurosci 23:5662-73.
48. Jones KR, Farinas I, Backus C, Reichardt LF. 1994. Targeted disruption of the BDNF gene perturbs brain and sensory neuron development but not motor neuron development. Cell 76:989-99.
49. Jovanovic JN, Thomas P, Kittler JT, Smart TG, Moss SJ. 2004. Brain-derived neurotrophic factor modulates fast synaptic inhibition by regulating GABA(A) receptor phosphorylation, activity, and cell-surface stability. J Neurosci 24:522-30.
50. Kaila K. 1994. Ionic basis of GABAA receptor channel function in the nervous system. Prog Neurobiol 42:489-537.
51. Kalanithi PS, Zheng W, Kataoka Y, DiFiglia M, Grantz H, Saper CB, and others. 2005. Altered parvalbumin-positive neuron distribution in basal ganglia of individuals with Tourette syndrome. Proc Natl Acad Sci U S A 102:13307-12.
52. Kim HG, Wang T, Olafsson P, Lu B. 1994. Neurotrophin 3 potentiates neuronal activity and inhibits gamma-aminobutyratergic synaptic transmission in cortical neurons. Proc Natl Acad Sci U S A 91:12341-5.
53. Klausberger T, Magill PJ, Marton LF, Roberts JD, Cobden PM, Buzsaki G, and others. 2003. Brain-state- and cell-type-specific firing of hippocampal interneurons in vivo. Nature 421:844-8.
54. Kohara K, Kitamura A, Adachi N, Nishida M, Itami C, Nakamura S, and others. 2003. Inhibitory but not excitatory cortical neurons require presynaptic brain-derived neurotrophic factor for dendritic development, as revealed by chimera cell culture. J Neurosci 23:6123-31.
55. Kokaia M, Ernfors P, Kokaia Z, Elmer E, Jaenisch R, Lindvall O. 1995. Suppressed epileptogenesis in BDNR mutant mice. Exp Neurol 133:215-24.
56. Lewis DA, Hashimoto T, Volk DW 2005. Cortical inhibitory neurons and schizophrenia. Nat Rev Neurosci 6:312-24.
57. Lewis DA, Lieberman JA. 2000. Catching up on schizophrenia: natural history and neurobiology. Neuron 28:325-34.
58. Lu B. 2003. BDNF and activity-dependent synaptic modulation. Learn Mem 10:86-98.
59. Lu B, Pang PT, Woo NH. 2005. The yin and yang of neurotrophin action. Nat Rev Neurosci 6:603-14.
60. Markram H, Toledo-Rodriguez M, Wang Y, Gupta A, Silberberg G, Wu C. 2004. Interneurons of the neocortical inhibitory system. Nat Rev Neurosci 5:793-807.
61. Marty S, Berninger B, Carroll P, Thoenen H. 1996. GABAergic stimulation regulates the phenotype of hippocampal interneurons through the regulation of brain-derived neurotrophic factor. Neuron 16:565-70.
62. Marty S, Wehrle R, Sotelo C. 2000. Neuronal activity and brain-derived neurotrophic factor regulate the density of inhibitory synapses in organotypic slice cultures of postnatal hippocampus. J Neurosci 20:8087-95.
63. Mizoguchi Y, Ishibashi H, Nabekura J. 2003. The action of BDNF on GABA(A) currents changes from potentiating to suppressing during maturation of rat hippocampal CAl pyramidal neurons. J Physiol 548:703-9.
64. Mizoguchi Y, Kanematsu T, Hirata M, Nabekura J. 2003. A rapid increase in the total number of cell surface functional GABAA receptors induced by brain-derived neurotrophic factor in rat visual cortex. J Biol Chem 278:44097-102.
65. Mizuno K, Caraahan J, Nawa H. 1994. Brain-derived neurotrophic factor promotes differentiation of striatal GABAergic neurons. Dev Biol 165:243-56.
66. Monteggia LM, Barrot M, Powell CM, Berton O, Galanis V, Gemelli T, and others. 2004. Essential role of brain-derived neurotrophic factor in adult hippocampal function. Proc Natl Acad Sci U S A 101:10827-32.
67. Moss SJ, Smart TG. 2001. Constructing inhibitory synapses. Nat Rev Neurosci 2:240-50.
68. Obeso JA, Rodriguez-Oroz MC, Lanciego JL, Rodriguez Diaz M. 2004. How does Parkinson's disease begin? The role of compensatory mechanisms. Trends Neurosci 27:125-7; author reply 127-8.
69. O'Donovan MJ. 1999. The origin of spontaneous activity in developing networks of the vertebrate nervous system. Curr Opin Neurobiol 9:94-104.
70. Patz S, Grabert J, Gorba T, Wirth MJ, Wahle P. 2004. Parvalbumin expression in visual cortical interneurons depends on neuronal activity and TrkB ligands during an early period of postnatal development. Cereb Cortex 14:342-51.
71. Perlstein WM, Carter CS, Noll DC, Cohen JD. 2001. Relation of prefrontal cortex dysfunction to working memory and symptoms in schizophrenia. Am J Psychiatry 158:1105-13.
72. Petroff OA. 2002. GABA and glutamate in the human brain. Neuroscientist 8:562-73.
73. Pierri JN, Chaudry AS, Woo TU, Lewis DA. 1999. Alterations in chandelier neuron axon terminals in the prefrontal cortex of schizophrenic subjects. Am J Psychiatry 156:1709-19.
74. Polleux F, Whitford KL, Dijkhuizen PA, Vitalis T, Ghosh A. 2002. Control of cortical interneuron migration by neurotrophins and PI3-kinase signaling. Development 129:3147-60.
75. Poo MM. 2001. Neurotrophins as synaptic modulators. Nat Rev Neurosci 2:24-32.
76. 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 23:622-31.
77. Rao SG, Williams GV, Goldman-Rakic PS. 1999. Isodirectional tuning of adjacent interneurons and pyramidal cells during working memory: evidence for microcolumnar organization in PFC. J Neurophysiol 81:1903-16.
78. Rao SG, Williams GV, Goldman-Rakic PS. 2000. Destruction and creation of spatial tuning by disinhibition: GABA(A) blockade of prefrontal cortical neurons engaged by working memory. J Neurosci 20:485-94.
79. Reynolds GP, Zhang ZJ, Beasley CL. 2001. Neurochemical correlates of cortical GABAergic deficits in schizophrenia: selective losses of calcium binding protein immunoreactivity. Brain Res Bull 55:579-84.
80. Rico B, Xu B, Reichardt LF. 2002. TrkB receptor signaling is required for establishment of GABAergic synapses in the cerebellum. Nat Neurosci 5:225-33.
81. Rivera C, Li H, Thomas-Crusells J, Lahtinen H, Viitanen T, Nanobashvili A, and others. 2002. BDNF-induced TrkB activation down-regulates the K+-Cl- cotransporter KCC2 and impairs neuronal Cl- extrusion. J Cell Biol 159:747-52.
82. Sawaguchi T, Matsumura M, Kubota K. 1988. Delayed response deficit in monkeys by locally disturbed prefrontal neuronal activity by bicuculline. Behav Brain Res 31:193-8.
83. Schwaller B, Tetko IV, Tandon P, Silveira DC, Vreugdenhil M, Henzi T, and others. 2004. Parvalbumin deficiency affects network properties resulting in increased susceptibility to epileptic seizures. Mol Cell Neurosci 25:650-63.
84. Seil FJ. 1999. BDNF and NT-4, but not NT-3, promote development of inhibitory synapses in the absence of neuronal activity. Brain Res 818:561-4.
85. Seil FJ, Drake-Baumann R. 2000. TrkB receptor ligands promote activity-dependent inhibitory synaptogenesis. J Neurosci 20:5367-73.
86. Sillito AM. 1979. Inhibitory mechanisms influencing complex cell orientation selectivity and their modification at high resting discharge levels. J Physiol 289:33-53.
87. Singer W, Gray CM. 1995. Visual feature integration and the temporal correlation hypothesis. Annu Rev Neurosci 18:555-86.
88. Spencer KM, Nestor PG, Niznikiewicz MA, Salisbury DF, Shenton ME, McCarley RW. 2003. Abnormal neural synchrony in schizophrenia. J Neurosci 23:7407-11.
89. Tallon-Baudry C, Bertrand O, Peronnet F, Pernier J. 1998. Induced gamma-band activity during the delay of a visual short-term memory task in humans. J Neurosci 18:4244-54.
90. Tamas G, Buhl EH, Lorincz A, Somogyi P. 2000. Proximally targeted GABAergic synapses and gap junctions synchronize cortical interneurons. Nat Neurosci 3:366-71.
91. Tanaka T, Saito H, Matsuki N. 1997. Inhibition of GABAA synaptic responses by brain-derived neurotrophic factor (BDNF) in rat hippocampus. J Neurosci 17:2959-66.
92. Toyooka K, Asama K, Watanabe Y, Muratake T, Takahashi M, Someya T, and others. 2002. Decreased levels of brain-derived neurotrophic factor in serum of chronic schizophrenic patients. Psychiatry Res 110:249-57.
93. Vicario-Abejon C, Collin C, McKay RD, Segal M. 1998. Neurotrophins induce formation of functional excitatory and inhibitory synapses between cultured hippocampal neurons. J Neurosci 18:7256-71.
94. Volk DW, Austin MC, Pierri JN, Sampson AR, Lewis DA. 2000. Decreased glutamic acid decarboxylase67 messenger RNA expression in a subset of prefrontal cortical gamma-aminobutyric acid neurons in subjects with schizophrenia. Arch Gen Psychiatry 57:237-45.
95. Wang Y, Fujita I, Murayama Y 2000. Neuronal mechanisms of selectivity for object features revealed by blocking inhibition in inferotemporal cortex. Nat Neurosci 3:807-13.
96. Wardle RA, Poo MM. 2003. Brain-derived neurotrophic factor modulation of GABAergic synapses by postsynaptic regulation of chloride transport. J Neurosci 23:8722-32.
97. Weickert CS, Hyde TM, Lipska BK, Herman MM, Weinberger DR, Kleinman JE. 2003. Reduced brain-derived neurotrophic factor in prefrontal cortex of patients with schizophrenia. Mol Psychiatry 8:592-610.
98. Weickert CS, Ligons DL, Romanczyk T, Ungaro G, Hyde TM, Herman MM, and others. 2005. Reductions in neurotrophin receptor mRNAs in the prefrontal cortex of patients with schizophrenia. Mol Psychiatry 10:637-50.
99. Weinberger DR, Berman KF, Zee RF. 1986. Physiologic dysfunction of dorsolateral prefrontal cortex in schizophrenia: I. Regional cerebral blood flow evidence. Arch Gen Psychiatry 43:114-24.
100. Wilson FA, O'Scalaidhe SP, Goldman-Rakic PS. 1994. Functional synergism between putative gamma-aminobutyrate-containing neurons and pyramidal neurons in prefrontal cortex. Proc Natl Acad Sci U S A 91:4009-13.
101. Wirth MJ, Brun A, Grabert J, Patz S, Wahle P. 2003. Accelerated dendritic development of rat cortical pyramidal cells and interneurons after biolistic transfection with BDNF and NT4/5. Development 130:5827-38.
102. Wittner L, Magloczky Z, Borhegyi Z, Halasz P, Toth S, Eross L, and others. 2001. Preservation of perisomatic inhibitory input of granule cells in the epileptic human dentate gyrus. Neuroscience 108:587-600.
103. Wonders C, Anderson SA. 2005. Cortical interneurons and their origins. Neuroscientist 11:199-205.
104. Woo TU, Whitehead RE, Melchitzky DS, Lewis DA. 1998. A subclass of prefrontal gamma-aminobutyric acid axon terminals are selectively altered in schizophrenia. Proc Natl Acad Sci U S A 95:5341-6.
105. Xu B, Zang K, Ruff NL, Zhang YA, McConnell SK, Stryker MP, and others. 2000. Cortical degeneration in the absence of neurotrophin signaling: dendritic retraction and neuronal loss after removal of the receptor TrkB. Neuron 26:233-45.
106. Yamada MK, Nakanishi K, Ohba S, Nakamura T, Ikegaya Y, Nishiyama N, and others. 2002. Brain-derived neurotrophic factor promotes the maturation of GABAergic mechanisms in cultured hippocampal neurons. J Neurosci 22:7580-5.
107. Ylinen A, Soltesz I, Bragin A, Penttonen M, Sik A, Buzsaki G. 1995. Intracellular correlates of hippocampal theta rhythm in identified pyramidal cells, granule cells, and basket cells. Hippocampus 5:78-90.