Altered cortical GABA neurotransmission in schizophrenia: Insights into novel therapeutic strategies

Current Pharmaceutical Biotechnology

Volumn 13, Issue 8, 2012, Pages 1557-1562

  Stan, Ana D ^a   Lewis, David A ^a  

^a UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

Basket neuron; Chandelier neuron; GABA A receptor; Parvalbumin; Prefrontal cortex

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR ALPHA2; PARVALBUMIN;

ARTICLE; AUTOPSY; COGNITIVE DEFECT; HUMAN; IMMUNOREACTIVITY; NEOCORTEX; NERVE ENDING; NEUROTRANSMISSION; PATHOPHYSIOLOGY; PREFRONTAL CORTEX; PRESYNAPTIC NERVE; PYRAMIDAL NERVE CELL; SCHIZOPHRENIA; SYNAPSE;

ANIMALS; ANTIPSYCHOTIC AGENTS; COGNITION DISORDERS; GAMMA-AMINOBUTYRIC ACID; HUMANS; PREFRONTAL CORTEX; SCHIZOPHRENIA; SYNAPTIC TRANSMISSION;

EID: 84862605801     PISSN: 13892010     EISSN: 18734316     Source Type: Journal    
DOI: 10.2174/138920112800784925     Document Type: Article

References (80)

1. Lewis, D.A.; Lieberman, J.A. Catching up on schizophrenia: natural history and neurobiology. Neuron, 2000, 28, 325-334.
2. Lewis, D.A.; Sweet, R.A. Schizophrenia from a neural circuitry perspective: advancing toward rational pharmacological therapies. J. Clin. Invest., 2009, 119(4), 706-716.
3. Elvevag, B.; Goldberg, T.E. Cognitive impairment in schizophrenia is the core of disorder. Crit. Rev. Neurobiol., 2000, 14(1), 1-21.
4. Gold, J.M. Cognitive deficits as treatment targets in schizophrenia. Schizophr. Res., 2004 72(1), 21-28.
5. Green, M.F. What are the functional consequences of neurocognitive deficits in schizophrenia? Am. J. Psychiatry, 1996, 153, 321-330.
6. Tan, H.Y.; Choo, W.C.; Fones, C.S.; Chee, M.W. FMRI study of maintenance and manipulation processes within working memory in first-episode schizophrenia. Am. J. Psychiatry, 2005, 162(10), 1849-1858.
7. Cannon, T.D.; Glahn, D.C.; Kim, J.; Van Erp, T.G.; Karlsgodt, K.; Cohen, M.S.; Nuechterlein, K.H.; Bava, S.; Shirinyan, D. Dorsolateral prefrontal cortex activity during maintenance and manipulation of information in working memory in patients with schizophrenia. Arch. Gen. Psychiatry, 2005, 62(10), 1071-1080.
8. Van Snellenberg, J.X.; Torres, I.J.; Thornton, A.E. Functional neuroimaging of working memory in schizophrenia: task performance as a moderating variable. Neuropsychology, 2006, 20(5), 497-510.
9. Minzenberg, M.J.; Laird, A.R.; Thelen, S.; Carter, C.S.; Glahn, D.C. Meta-analysis of 41 functional neuroimaging studies of executive function in schizophrenia. Arch. Gen. Psychiatry, 2009, 66(8), 811-822.
10. MacDonald, A.W., III; Carter, C.S.; Kerns, J.G.; Ursu, S.; Barch, D.M.; Holmes, A.J.; Stenger, V.A.; Cohen, J.D. Specificity of prefrontal dysfunction and context processing deficits to schizophrenia in never-medicated patients with first-episode psychosis. Am. J. Psychiatry, 2005, 162(3), 475-484.
11. Barch, D.M.; Sheline, Y.I.; Csernansky, J.G.; Snyder, A.Z. Working memory and prefrontal cortex dysfunction: specificity to schizophrenia compared with major depression. Biol. Psychiatry, 2003, 53, 376-384.
12. Reichenberg, A.; Caspi, A.; Harrington, H.; Houts, R.; Keefe, R.S.; Murray, R.M.; Poulton, R.; Moffitt, T.E. Static and dynamic cognitive deficits in childhood preceding adult schizophrenia: a 30-year study. Am. J. Psychiatry, 2010, 167(2), 160-169.
13. Bird, E.D.; Spokes, E.G.; Barnes, J.; Mackay, A.V.; Iversen, L.L.; Shepherd, M. Glutamic-acid decarboxylase in schizophrenia. Lancet, 1978, 1(8056), 156.
14. Simpson, M.D.C.; Slater, P.; Deakin, J.F.W.; Royston, M.C.; Skan, W.J. Reduced GABA uptake sites in the temporal lobe in schizophrenia. Neurosci. Lett., 1989, 107, 211-215.
15. Hanada, S.; Mita, T.; Nishino, N.; Tanaka, C. [3H]muscimol binding sites increased in autopsied brains of chronic schizophrenics. Life Sci., 1987, 40, 239-266.
16. Benes, F.M.; Vincent, S.L.; Marie, A.; Khan, Y. Up-regulation of GABA receptor binding on neurons of the prefrontal cortex in schizophrenic subjects. Neuroscience, 1996, 75, 1021-1031.
17. Asada, H.; Kawamura, Y.; Maruyama, K.; Kume, H.; Ding, R.; Ji, F.Y.; Kanbara, N.; Kuzume, H.; Sanbo, M.; Yagi, T.; Obata, K. Mice lacking the 65 kDa isoform of glutamic acid decarboxylase (GAD65) maintain normal levels of GAD67 and GABA in their brains but are susceptible to seizures. Biochem. Biophys. Res. Comm., 1996, 229, 891-895.
18. Asada, H.; Kawamura, Y.; Maruyama, K.; Kume, H.; Ding, R.; Kanbara, N.; Kuzume, H.; Sanbo, M.; Yagi, T.; Obata, K. Cleft palate and decreased brain gamma-aminobutyric acid in mice lacking the 67-kDa isoform of glutamic acid decarboxylase. Proc. Natl. Acad. Sci. USA, 1997, 94, 6496-6499.
19. Akbarian, S.; Kim, J.J.; Potkin, S.G.; Hagman, J.O.; Tafazzoli, A.; Bunney, Jr. W.E.; Jones, E.G. Gene expression for glutamic acid decarboxylase is reduced without loss of neurons in prefrontal cortex of schizophrenics. Arch. Gen. Psychiatry, 1995, 52, 258-266.
20. Volk, D.W.; Austin, M.C.; Pierri, J.N.; Sampson, A.R.; Lewis, D.A. Decreased glutamic acid decarboxylase67 messenger RNA expression in a subset of prefrontal cortical gamma-aminobutyric acid neurons in subjects with schizophrenia. Arch. Gen. Psychiatry, 2000, 57(3), 237-245.
21. Guidotti, A.; Auta, J.; Davis, J.M.; Gerevini, V.D.; Dwivedi, Y.; Grayson, D.R.; Impagnatiello, F.; Pandey, G.; Pesold, C.; Sharma, R.; Uzunov, D.; Costa, E. Decrease in reelin and glutamic acid decarboxylase67 (GAD67) expression in schizophrenia and bipolar disorder: a postmortem brain study. Arch. Gen. Psychiatry, 2000, 57, 1061-1069.
22. Mirnics, K.; Middleton, F.A.; Marquez, A.; Lewis, D.A.; Levitt, P. Molecular characterization of schizophrenia viewed by microarray analysis of gene expression in prefrontal cortex. Neuron, 2000, 28, 53-67.
23. Vawter, M.P.; Crook, J.M.; Hyde, T.M.; Kleinman, J.E.; Weinberger, D.R.; Becker, K.G.; Freed, W.J. Microarray analysis of gene expression in the prefrontal cortex in schizophrenia: a preliminary study. Schizophr. Res., 2002, 58, 11-20.
24. Hashimoto, T.; Bergen, S.E.; Nguyen, Q.L.; Xu, B.; Monteggia, L.M.; Pierri, J.N.; Sun, Z.; Sampson, A.R.; Lewis, D.A. Relationship of brain-derived neurotrophic factor and ist receptor TrkB to altered inhibitory prefrontal circuitry in schizophrenia. J. Neurosci., 2005, 25(2), 372-383.
25. Hashimoto, T.; Arion, D.; Unger, T.; Maldonado-Aviles, J.G.; Morris, H.M.; Volk, D.W.; Mirnics, K.; Lewis, D.A. Alterations in GABA-related transcriptome in the dorsolateral prefrontal cortex of subjects with schizophrenia. Mol. Psychiatry, 2008, 13(2), 147-161.
26. Hashimoto, T.; Bazmi, H.H.; Mirnics, K.; Wu, Q.; Sampson, A.R.; Lewis, D.A. Conserved regional patterns of GABA-related transcript expression in the neocortex of subjects with schizophrenia. Am. J. Psychiatry, 2008, 165(4), 479-489.
27. Straub, R.E.; Lipska, B.K.; Egan, M.F.; Goldberg, T.E.; Callicott, J.H.; Mayhew, M.B.; Vakkalanka, R.K.; Kolachana, B.S.; Kleinman, J.E.; Weinberger, D.R. Allelic variation in GAD1 (GAD67) is associated with schizophrenia and influences cortical function and gene expression. Mol. Psychiatry, 2007, 12(9), 854-869.
28. Mellios, N.; Huang, H.S.; Baker, S.P.; Galdzicka, M.; Ginns, E.; Akbarian, S. Molecular determinants of dysregulated GABAergic gene expression in the prefrontal cortex of subjects with schizophrenia. Biol. Psychiatry, 2009, 65(12), 1006-1014.
29. Duncan, C.E.; Webster, M.J.; Rothmond, D.A.; Bahn, S.; Elashoff, M.; Shannon Weickert, C. Prefrontal GABA(A) receptor alphasubunit expression in normal postnatal human development and schizophrenia. J. Psychiatr. Res., 2010, 44(10), 673-681.
30. Curley, A.A.; Arion, D.; Volk, D.W.; Asafu-Adjei, J.K.; Sampson, A.R.; Fish, K.N.; Lewis, D.A. Cortical deficits of glutamic acid decarboxylase 67 expression in schizophrenia: clinical, protein, and cell type-specific features. Am. J. Psychiatry, 2011, 168(9), 921-929.
31. Woo, T.-U.; Walsh, J.P.; Benes, F.M. Density of glutamic acid decarboxylase 67 messenger RNA-containing neurons that express the N-methyl-D-aspartate receptor subunit NR2A in the anterior cingulate cortex in schizophrenia and bipolar disorder. Arch. Gen. Psychiatry, 2004, 61(7), 649-657.
32. Impagnatiello, F.; Guidotti, A.R.; Pesold, C.; Dwivedi, Y.; Caruncho, H.; Pisu, M.G.; Uzunov, D.P.; Smalheiser, N.R.; Davis, J.M.; Pandey, G.N.; Pappas, G.D.; Teuting, P.; Sharma, R.P.; Costa, E. A decrease of reelin expression as a putative vulnerability factor in schizophrenia. Proc. Natl. Acad. Sci. USA, 1998, 95, 15718-15723.
33. Thompson, M.; Weickert, C.S.; Wyatt, E.; Webster, M.J. Decreased glutamic acid decarboxylase(67) mRNA expression in multiple brain areas of patients with schizophrenia and mood disorders. J. Psychiatr. Res., 2009, 43(11), 970-977.
34. Ohnuma, T.; Augood, S.J.; Arai, H.; McKenna, P.J.; Emson, P.C. Measurment of GABAergic parameters in the prefrontal cortex in schizophrenia: focus on GABA content, GABA(A) receptor alpha-1 subunit messenger RNA and human GABA transporter-1 (HGAT-1) messenger RNA expression. Neuroscience, 1999, 93, 441-448.
35. Volk, D.W.; Austin, M.C.; Pierri, J.N.; Sampson, A.R.; Lewis, D.A. GABA transporter-1 mRNA in the prefrontal cortex in schizophrenia: decreased expression in a subset of neurons. Am. J. Psychiatry, 2001, 158, 256-265.
36. Ascoli, G.A.; Alonso-Nanclares, L.; Erson, S.A.; Barrionuevo, G.; Benavides-Piccione, R.; Burkhalter, A.; Buzsaki, G.; Cauli, B.; DeFelipe, J.; Fairen, A.; Feldmeyer, D.; Fishell, G.; Fregnac, Y.; Freund, T.F.; Gardner, D.; Gardner, E.P.; Goldberg, J.H.; Helmstaedter, M.; Hestrin, S.; Karube, F.; Kisvarday, Z.F.; Lambolez, B.; Lewis, D.A.; Marin, O.; Markram, H.; Munoz, A.; Packer, A.; Petersen, C.C.; Rockland, K.S.; Rossier, J.; Rudy, B.; Somogyi, P.; Staiger, J.F.; Tamas, G.; Thomson, A.M.; Toledo-Rodriguez, M.; Wang, Y.; West, D.C.; Yuste, R. Petilla terminology: nomenclature of features of GABAergic interneurons if the cerebral cortex. Nat. Rev. Neurosci., 2008, 9(7), 557-568.
37. Condé, F.; Lund, J.S.; Jacobowitz, D.M.; Baimbridge, K.G.; Lewis, D.A. Local circuit neurons immunoreactive for calretinin, calbindin D-28k or parvalbumin in monkey prefrontal cortex: distribution and morphology. J. Comp. Neurol., 1994, 341, 95-116.
38. Gabbott, P.L.A.; Bacon, S.J. Local circuit neurons in the medial prefrontal cortex (areas 24a,b,c, 25 and 32) in the monkey: II. Quantitative areal and laminar distributions. J. Comp. Neurol., 1996, 364, 609-636.
39. DeFelipe, J. Types of neurons, synaptic connections and chemical characteristics of cells immunoreactive for calbindin-D28K, parvalbumin and calretinin in the neocortex. J. Chem. Neuroanat., 1997, 14, 1-19.
40. Krimer, L.S.; Zaitsev, A.V.; Czanner, G.; Kroner, S.; Gonzalez-Burgos, G.; Povysheva, N.V.; Iyengar, S.; Barrionuevo, G.; Lewis, D.A. Cluster analysis-based physiological classification and morphological properties of inhibitory neurons in layers 2-3 of monkey dorsolateral prefrontal cortex. J. Neurophysiol., 2005, 94(5), 3009-3022.
41. Zaitsev, A.V.; Gonzalez-Burgos, G.; Povysheva, N.V.; Kroner, S.; Lewis, D.A.; Krimer, L.S. Localization of calcium-binding proteins in physiologically and morphologically characterized interneurons of monkey dorsolateral prefrontal cortex. Cereb Cortex, 2005, 15(8), 1178-1186.
42. Zaitsev, A.V.; Povysheva, N.V.; Gonzalez-Burgos, G.; Rotaru, D.; Fish, K.N.; Krimer, L.S.; Lewis, D.A. Interneuron diversity in layers 2-3 of monkey prefrontal cortex. Cereb Cortex, 2009, 19(7), 1597-1615.
43. Williams, S.M.; Goldman-Rakic, P.S.; Leranth, C. The synaptology of parvalbumin-immunoreactive neurons in the primate prefrontal cortex. J. Comp. Neurol., 1992, 320, 353-369.
44. Melchitzky, D.S.; Sesack, S.R.; Lewis, D.A. Parvalbuminimmunoreactive axon terminals in macaque monkey and human prefrontal cortex: laminar, regional, and target specificity of type I and type II synapses. J. Comp. Neurol., 1999, 408, 11-22.
45. Melchitzky, D.S.; Eggan, S.M.; Lewis, D.A. Synaptic targets of calretinin-containing axon terminals in macaque monkey prefrontal cortex. Neuroscience, 2005, 130(1), 185-195.
46. DeLima, A.D.; Morrison, J.H. Ultrastructural analysis of somatostatin-immunoreactive neurons and synapses in the temporal and occipital cortex of the macaque monkey. J. Comp. Neurol., 1989, 283, 212-227.
47. Kawaguchi, Y.; Kubota, Y. Physiological and morphological identification of somatostatin- or vasoactive intestinal polypeptidecontaining cells among GABAergic cell subtypes in rat frontal cortex. J. Neurosci., 1996, 16, 2701-2715.
48. Ma, Y.; Hu, H.; Berrebi, A.S.; Mathers, P.H.; Agmon, A. Distinct subtypes of somatostatin-containing neocortical interneurons revealed in transgenic mice. J. Neurosci., 2006, 26(19), 5069-5082.
49. Hashimoto, T.; Volk, D.W.; Eggan, S.M.; Mirnics, K.; Pierri, J.N.; Sun, Z.; Sampson, A.R.; Lewis, D.A. Gene expression deficits in a subclass of GABA neurons in the prefrontal cortex of subjects with schizophrenia. J. Neurosci., 2003, 23, 6315-6326.
50. Woo, T.-U.; Miller, J.L.; Lewis, D.A. Schizophrenia and the parvalbumin- containing class of cortical local circuit neurons. Am. J. Psychiatry, 1997, 154(7), 1013-1015.
51. Tooney, P.A.; Chahl, L.A. Neurons expressing calcium-binding proteins in the prefrontal cortex in schizophrenia. Prog. Neuropsychopharmacol. Biol. Psychiatry, 2004, 28(2), 273-278.
52. Beasley, C.L.; Zhang, Z.J.; Patten, I.; Reynolds, G.P. Selective deficits in prefrontal cortical GABAergic neurons in schizophrenia defined by the presence of calcium-binding proteins. Biol. Psychiatry, 2002, 52, 708-715.
53. Reynolds, G.P.; Beasley, C.L.; Zhang, Z.J. Understanding the neurotransmitter pathology of schizophrenia: selective deficits of subtypes of cortical GABAergic neurons. J. Neural Transm., 2002, 109(5-6), 881-889.
54. Beasley, C.L.; Reynolds, G.P. Parvalbumin-immunoreactive neurons are reduced in the prefrontal cortex of schizophrenics. Schizophr. Res., 1997, 24, 349-355.
55. Thune, J.J.; Uylings, H.B.M.; Pakkenberg, B. No deficit in total number of neurons in the prefrontal cortex in schizophrenics. J. Psychiatr. Res., 2001, 35, 15-21.
56. Palkovits, M.; Mezey, E.; Hamori, J.; Szentagothai, J. Quantitative histological analysis of the cerebellar nuclei in the cat. I. Numerical data on cells and on synapses. Exp. Brain Res., 1977, 28(1-2), 189-209.
57. Somogyi, P. A specific 'axo-axonal' interneuron in the visual cortex of the rat. Brain Res., 1977, 136, 345-350.
58. Freund, T.F.; Buzsaki, G. Interneurons of the hippocampus. Hippocampus, 1996, 6(4), 347-470.
59. Woo, T.-U.; Whitehead, R.E.; Melchitzky, D.S.; Lewis, D.A. A subclass of prefrontal gamma-aminobutyric acid axon terminals are selectively altered in schizophrenia. Proc. Natl. Acad. Sci. USA, 1998, 95(9), 5341-5346.
60. Pierri, J.N.; Chaudry, A.S.; Woo, T.-U.; Lewis, D.A. Alterations in chandelier neuron axon terminals in the prefrontal cortex of schizophrenic subjects. Am. J. Psychiatry, 1999, 156(11), 1709-1719.
61. Nusser, Z.; Sieghart, W.; Benke, D.; Fritschy, J.-M.; Somogyi, P. Differential synaptic localization of two major gamma-aminobutyric acid type A receptor alpha subunits on hippocampal pyramidal cells. Proc. Natl. Acad. Sci. USA, 1996, 93, 11939-11944.
62. Volk, D.W.; Pierri, J.N.; Fritschy, J.-M.; Auh, S.; Sampson, A.R.; Lewis, D.A. Reciprocal alterations in pre- and postsynaptic inhibitory markers at chandelier cell inputs to pyramidal neurons in schizophrenia. Cereb. Cortex, 2002, 12, 1063-1070.
63. Collin, T.; Chat, M.; Lucas, M.G.; Moreno, H.; Racay, P.; Schwaller, B.; Marty, A.; Llano, I. Developmental changes in parvalbumin regulate presynaptic Ca2+ signaling. J. Neurosci., 2005, 25(1), 96-107.
64. Muller, M.; Felmy, F.; Schwaller, B.; Schneggenburger, R. Parvalbumin is a mobile presynaptic Ca2+ buffer in the calyx of held that accelerates the decay of Ca2+ and short-term facilitation. J. Neurosci., 2007, 27(9), 2261-2271.
65. Vreugdenhil, M.; Jefferys, J.G.; Celio, M.R.; Schwaller, B. Parvalbumin- deficiency facilitates repetitive IPSCs and gamma oscillations in the hippocampus. J. Neurophysiol., 2003, 89(3), 1414-1422.
66. Overstreet, L.S.; Westbrook, G.L. Synapse density regulates independence at unitary inhibitory synapses. J. Neurosci., 2003, 23(7), 2618-2626.
67. Lewis, D.A.; Volk, D.W.; Hashimoto, T. Selective alterations in prefrontal cortical GABA neurotransmission in schizophrenia: a novel target for the treatment of working memory dysfunction. Psychopharmacology, 2004, 174(1), 143-150.
68. Carpenter, W.T., Jr.; Buchanan, R.W.; Kirkpatrick, B.; Breier, A.F. Diazepam treatment of early signs of exacerbation in schizophrenia. Am. J. Psychiatry, 1999, 156, 299-303.
69. Lewis, D.A.; Cho, R.Y.; Carter, C.S.; Eklund, K.; Forster, S.; Kelly, M.A.; Montrose, D. Subunit-selective modulation of GABA type A receptor neurotransmission and cognition in schizophrenia. Am. J. Psychiatry, 2008, 165(12), 1585-1593.
70. Castner, S.A.; Arriza, J.L.; Roberts, J.C.; Mrzljak, L.; Christian, E.P.; Williams, G.V. Reversal of ketamine-induced working memory impairments by the GABAAalpha2/3 agonist TPA023. Biol. Psychiatry, 2010, 67(10), 998-1001.
71. de Haas, S.L.; de Visser, S.J.; van der Post, J.P.; de Smet, M.; Schoemaker, R.C.; Rijnbeek, B.; Cohen, A.F.; Vega, J.M.; Agrawal, N.G.; Goel, T.V.; Simpson, R.C.; Pearson, L.K.; Li, S.; Hesney, M.; Murphy, M.G.; van Gerven, J.M. Pharmacodynamic and pharmacokinetic effects of TPA023, a GABA(A) alpha(2,3) subtype-selective agonist, compared to lorazepam and placebo in healthy volunteers. J. Psychopharmacol., 2007, 21(4), 374-383.
72. Stein, V.; Nicol, R.A. GABA generates excitement. Neuron, 2003, 37, 375-378.
73. Szabadics, J.; Varga, C.; Molnar, G.; Olah, S.; Barzo, P.; Tamas, G. Excitatory effect of GABAergic axo-axonic cells in cortical microcircuits. Science, 2006, 311(5758), 233-235.
74. Molnar, G.; Olah, S.; Komlosi, G.; Fule, M.; Szabadics, J.; Varga, C.; Barzo, P.; Tamas, G. Complex events initiated by individual spikes in the human cerebral cortex. PLoS Biol., 2008, 6(9), e222.
75. Khirug, S.; Yamada, J.; Afzalov, R.; Voipio, J.; Khiroug, L.; Kaila, K. GABAergic depolarization of the axon initial segment in cortical principal neurons is caused by the Na-K-2Cl cotransporter NKCC1. J. Neurosci., 2008, 28(18), 4635-4639.
76. Glickfeld, L.L.; Roberts, J.D.; Somogyi, P.; Scanziani, M. Interneurons hyperpolarize pyramidal cells along their entire somatodendritic axis. Nat. Neurosci., 2009, 12(1), 21-23.
77. Woodruff, A.; Xu, Q.; Anderson, S.A.; Yuste, R. Depolarizing effect of neocortical chandelier neurons. Front Neural. Circuits., 2009, 3, 15.
78. Lewis, D.A.; Hashimoto, T.; Volk, D.W. Cortical inhibitory neurons and schizophrenia. Nat. Rev. Neurosci., 2005, 6(4), 312-324.
79. Lewis, D.A.; Gonzalez-Burgos, G. Neuroplasticity of neocortical circuits in schizophrenia. Neuropsychopharmacol. Rev., 2008, 33(1), 141-165.
80. Lewis, D. The chandelier neuron in schizophrenia. Dev. Neurobiol., 2011, 71(1), 118-127.