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Neural Plasticity
Volume 2011, Article ID 723184, 24 pages
http://dx.doi.org/10.1155/2011/723184
Review Article

GABA Neuron Alterations, Cortical Circuit Dysfunction and Cognitive Deficits in Schizophrenia

Translational Neuroscience Program, Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA 15261, USA

Received 16 February 2011; Accepted 1 May 2011

Academic Editor: Tommaso Pizzorusso

Copyright © 2011 Guillermo Gonzalez-Burgos et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Citations to this Article [134 citations]

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  • Kevin J. Mitchell, Z. Josh Huang, Bita Moghaddam, and Akira Sawa, “Following the genes: a framework for animal modeling of psychiatric disorders,” Bmc Biology, vol. 9, 2011. View at Publisher · View at Google Scholar
  • Michelle M McCarthy, ShiNung Ching, Miles A Whittington, and Nancy Kopell, “Dynamical changes in neurological diseases and anesthesia,” Current Opinion in Neurobiology, vol. 22, no. 4, pp. 693–703, 2012. View at Publisher · View at Google Scholar
  • Juan Song, Chun Zhong, Michael A. Bonaguidi, Gerald J. Sun, Derek Hsu, Yan Gu, Konstantinos Meletis, Z. Josh Huang, Shaoyu Ge, Grigori Enikolopov, Karl Deisseroth, Bernhard Luscher, Kimberly M. Christian, Guo-li Ming, and Hongjun Song, “Neuronal circuitry mechanism regulating adult quiescent neural stem-cell fate decision,” Nature, vol. 489, no. 7414, pp. 150–154, 2012. View at Publisher · View at Google Scholar
  • Jingyi Ma, Siew Kian Tai, and L. Stan Leung, “ Septohippocampal GABAergic neurons mediate the altered behaviors induced by n -methyl- D -aspartate receptor antagonists ,” Hippocampus, vol. 22, no. 12, pp. 2208–2218, 2012. View at Publisher · View at Google Scholar
  • Daniel P. Spiegel, Bruce C. Hansen, Winston D. Byblow, and Benjamin Thompson, “Anodal Transcranial Direct Current Stimulation Reduces Psychophysically Measured Surround Suppression in the Human Visual Cortex,” Plos One, vol. 7, no. 5, 2012. View at Publisher · View at Google Scholar
  • John A. Saunders, Michael J. Gandal, and Steve J. Siegel, “NMDA antagonists recreate signal-to-noise ratio and timing perturbations present in schizophrenia,” Neurobiology of Disease, vol. 46, no. 1, pp. 93–100, 2012. View at Publisher · View at Google Scholar
  • Sivan Subburaju, and Francine M. Benes, “Induction of the GABA Cell Phenotype: An In Vitro Model for Studying Neurodevelopmental Disorders,” Plos One, vol. 7, no. 3, 2012. View at Publisher · View at Google Scholar
  • Marc G. Caron, William C. Wetsel, Xiaodong Zhang, Peiyan Wong, Cecilia Chin Roei Chang, and Christine E. Marx, “Pregnenolone Rescues Schizophrenia-Like Behavior in Dopamine Transporter Knockout Mice,” Plos One, vol. 7, no. 12, 2012. View at Publisher · View at Google Scholar
  • Tomasz Gos, Johann Steiner, Hendrik Bielau, Henrik Dobrowolny, Karoline Guenther, Christian Mawrin, Maciej Krzyzanowski, Roman Hauser, Ralf Brisch, Hans-Gert Bernstein, Zbigniew Jankowski, Katharina Braun, and Bernhard Bogerts, “Differences between unipolar and bipolar I depression in the quantitative analysis of glutamic acid decarboxylase-immunoreactive neuropil,” European Archives Of Psychiatry And Clinical Neuroscience, vol. 262, no. 8, pp. 647–655, 2012. View at Publisher · View at Google Scholar
  • Joshua A. Gordon, and Holly Moore, “Charting a Course toward an Understanding of Schizophrenia,” Neuron, vol. 76, no. 3, pp. 465–467, 2012. View at Publisher · View at Google Scholar
  • Catherine L. Winchester, Brian J. Morris, Hiromitsu Ohzeki, Demetrius A. Vouyiouklis, Rhiannon Thompson, Josef M. Penninger, Keiji Yamagami, John D. Norrie, Robert Hunter, and Judith A. Pratt, “Converging evidence that sequence variations in the novel candidate gene MAP2K7 (MKK7) are functionally associated with schizophrenia,” Human Molecular Genetics, vol. 21, no. 22, pp. 4910–4921, 2012. View at Publisher · View at Google Scholar
  • Eric C. Donny, Tracy G. Taylor, Mark G. LeSage, Melissa Levin, Deanne M. Buffalari, Danielle Joel, and Alan F. Sved, “Impact of tobacco regulation on animal research: New perspectives and opportunities,” Nicotine and Tobacco Research, vol. 14, no. 11, pp. 1319–1338, 2012. View at Publisher · View at Google Scholar
  • Michael J. Minzenberg, and Cameron S. Carter, “Developing treatments for impaired cognition in schizophrenia,” Trends in Cognitive Sciences, vol. 16, no. 1, pp. 35–42, 2012. View at Publisher · View at Google Scholar
  • Bidisha Chattopadhyaya, and Graziella Di Cristo, “GABAergic circuit dysfunctions in neurodevelopmental disorders,” Frontiers in Psychiatry, vol. 3, no. MAY, 2012. View at Publisher · View at Google Scholar
  • S H Fatemi, T D Folsom, R J Rooney, and P D Thuras, “Expression of GABAA α2-, β1- and ɛ-receptors are altered significantly in the lateral cerebellum of subjects with schizophrenia, major depression and bipolar disorder,” Translational Psychiatry, vol. 3, no. 9, pp. e303, 2013. View at Publisher · View at Google Scholar
  • Suthicha Wuwongse, Sally Shuk-Yee Cheng, Ginger Tsz-Hin Wong, Clara Hiu-Ling Hung, Natalie Qishan Zhang, Yuen-Shan Ho, Andrew Chi-Kin Law, and Raymond Chuen-Chung Chang, “Effects of corticosterone and amyloid-beta on proteins essential for synaptic function: Implications for depression and Alzheimer’s disease,” Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease, 2013. View at Publisher · View at Google Scholar
  • Zhe Yu, Qi Fang, Xian Xiao, Yi-Zhi Wang, You-Qing Cai, Hui Cao, Gang Hu, Zhong Chen, Jian Fei, Neng Gong, and Tian-Le Xu, “GABA Transporter-1 Deficiency Confers Schizophrenia-Like Behavioral Phenotypes,” Plos One, vol. 8, no. 7, 2013. View at Publisher · View at Google Scholar
  • S H Fatemi, T D Folsom, R J Rooney, and P D Thuras, “mRNA and protein expression for novel GABAA receptors θ and ρ2 are altered in schizophrenia and mood disorders; relevance to FMRP-mGluR5 signaling pathway,” Translational Psychiatry, vol. 3, no. 6, pp. e271, 2013. View at Publisher · View at Google Scholar
  • Gregory B. Bissonette, Elizabeth M. Powell, and Matthew R. Roesch, “Neural structures underlying set-shifting: Roles of medial prefrontal cortex and anterior cingulate cortex,” Behavioural Brain Research, 2013. View at Publisher · View at Google Scholar
  • Frankie H. F. Lee, Clement C. Zai, Sabine P. Cordes, John C. Roder, and Albert H. C. Wong, “Abnormal interneuron development in disrupted-in-schizophrenia-1 L100P mutant mice,” Molecular Brain, vol. 6, 2013. View at Publisher · View at Google Scholar
  • Matilda Haas, Zhengdong Qu, Tae Hwan Kim, Ernesto Vargas, Kenneth Campbell, Steven Petrou, Seong-Seng Tan, Christopher A. Reid, and Julian Heng, “Perturbations in cortical development and neuronal network excitability arising from prenatal exposure to benzodiazepines in mice,” European Journal of Neuroscience, vol. 37, no. 10, pp. 1584–1593, 2013. View at Publisher · View at Google Scholar
  • Alkomiet Hasan, Kristina Misewitsch, Michael A. Nitsche, Oliver Gruber, Frank Padberg, Peter Falkai, and Thomas Wobrock, “Impaired Motor Cortex Responses in Non-Psychotic First-Degree Relatives of Schizophrenia Patients: A Cathodal tDCS Pilot Study,” Brain Stimulation, 2013. View at Publisher · View at Google Scholar
  • Cristina Bañuelos, Candi L. LaSarge, Joseph A. McQuail, John J. Hartman, Ryan J. Gilbert, Brandi K. Ormerod, and Jennifer L. Bizon, “Age-related changes in rostral basal forebrain cholinergic and GABAergic projection neurons: relationship with spatial impairment,” Neurobiology of Aging, vol. 34, no. 3, pp. 845–862, 2013. View at Publisher · View at Google Scholar
  • Hedi Hegyi, “GABBR1 has a HERV-W LTR in its regulatory region - a possible implication for schizophrenia,” Biology Direct, vol. 8, 2013. View at Publisher · View at Google Scholar
  • Eun-Shil Lee, and Chang-Jin Jeon, “Starburst amacrine cells express parvalbumin but not calbindin and calretinin in rabbit retina,” NeuroReport, vol. 24, no. 16, pp. 918–923, 2013. View at Publisher · View at Google Scholar
  • D. W. Meechan, H. L. H. Rutz, M. S. Fralish, T. M. Maynard, L. A. Rothblat, and A.- S. LaMantia, “Cognitive Ability is Associated with Altered Medial Frontal Cortical Circuits in the LgDel Mouse Model of 22q11.2DS,” Cerebral Cortex, 2013. View at Publisher · View at Google Scholar
  • Erica Zamberletti, Sarah Beggiato, Luca Steardo, Pamela Prini, Tiziana Antonelli, Luca Ferraro, Tiziana Rubino, and Daniela Parolaro, “Alterations of prefrontal cortex GABAergic transmission in the complex psychotic-like phenotype induced by adolescent delta-9-tetrahydrocannabinol exposure in rats,” Neurobiology of Disease, 2013. View at Publisher · View at Google Scholar
  • Edward Ram, Shani Raphaeli, and Avi Avital, “Prepubertal chronic stress and ketamine administration to rats as a neurodevelopmental model of schizophrenia symptomatology,” International Journal of Neuropsychopharmacology, vol. 16, no. 10, pp. 2307–2314, 2013. View at Publisher · View at Google Scholar
  • Daniel R. Thomases, Daryn K. Cass, and Kuei Y. Tseng, “Periadolescent Exposure to the NMDA Receptor Antagonist MK-801 Impairs the Functional Maturation of Local GABAergic Circuits in the Adult Prefrontal Cortex,” Journal Of Neuroscience, vol. 33, no. 1, pp. 26–U431, 2013. View at Publisher · View at Google Scholar
  • Chris M. Hempel, David J. Gerber, Michael Sivula, Ryan J. Babcock, Helen E. Gibson, Bing Li, Jeffrey R. Cottrell, David M. Rose, Kjesten A. Wiig, Pascal Laeng, Margaret E. Levin, Sung Hyun Kim, Kristen A. Richardson, Timothy A. Ryan, Jonathan M. Levenson, Crystle J. Ashford, and Karen A. Heindl, “Working Memory Impairment in Calcineurin Knock-out Mice Is Associated with Alterations in Synaptic Vesicle Cycling and Disruption of High-Frequency Synaptic and Network Activity in Prefrontal Cortex,” Journal Of Neuroscience, vol. 33, no. 27, pp. 10938–10949, 2013. View at Publisher · View at Google Scholar
  • Paola Imbrici, Diana Conte Camerino, and Domenico Tricarico, “Major channels involved in neuropsychiatric disorders and therapeutic perspectives,” Frontiers in Genetics, vol. 4, no. MAY, 2013. View at Publisher · View at Google Scholar
  • Qi Li, Wai Man Chan, John A. Rudd, Chun Mei Wang, Phoebe Y.H. Lam, Maria Sen Mun Wai, David M. Wood, Paul I. Dargan, and David T. Yew, “Ketamine,” Novel Psychoactive Substances, pp. 285–316, 2013. View at Publisher · View at Google Scholar
  • Chia-Chun Huang, Min-Chih Cheng, Ho-Min Tsai, Chih-Hao Lai, and Chia-Hsiang Chen, “Genetic analysis of GABRB3 at 15q12 as a candidate gene of schizophrenia,” Psychiatric Genetics, vol. 24, no. 4, pp. 151–157, 2014. View at Publisher · View at Google Scholar
  • Daniel R. Thomases, Daryn K. Cass, Jacqueline D. Meyer, Adriana Caballero, and Kuei Y. Tseng, “Early Adolescent MK-801 Exposure Impairs the Maturation of Ventral Hippocampal Control of Basolateral Amygdala Drive in the Adult Prefrontal Cortex,” Journal of Neuroscience, vol. 34, no. 27, pp. 9059–9066, 2014. View at Publisher · View at Google Scholar
  • Christine E. Marx, Jimmy Lee, Mythily Subramaniam, Attilio Rapisarda, Dianne C. T. Bautista, Edwin Chan, Jason D. Kilts, Robert W. Buchanan, Eu Pui Wai, Swapna Verma, Kang Sim, Jayaraman Hariram, Rajesh Jacob, Richard S. E. Keefe, and Siow Ann Chong, “Proof-of-concept randomized controlled trial of pregnenolone in schizophrenia,” Psychopharmacology, 2014. View at Publisher · View at Google Scholar
  • F. Riese, A. Gietl, N. Zölch, A. Henning, R. O’Gorman, A.M. . Kälin, S.E. Leh, A. Buck, G. Warnock, R.A.E. Edden, R. Luechinger, C. Hock, S. Kollias, and L. Michels, “Posterior cingulate GABA and glutamate+glutamine are reduced in amnestic mild cognitive impairment and are unrelated to amyloid deposition and APOE genotype,” Neurobiology of Aging, 2014. View at Publisher · View at Google Scholar
  • Sylvina M. Raver, and Asaf Keller, “Permanent suppression of cortical oscillations in mice after adolescent exposure to cannabinoids: Receptor mechanisms,” Neuropharmacology, 2014. View at Publisher · View at Google Scholar
  • Hong Lin, Fu-Chun Hsu, Bailey H. Baumann, Douglas A. Coulter, Stewart A. Anderson, and David R. Lynch, “Cortical parvalbumin GABAergic deficits with α7 nicotinic acetylcholine receptor deletion: implications for schizophrenia,” Molecular and Cellular Neuroscience, 2014. View at Publisher · View at Google Scholar
  • Jill R. Glausier, Sohei Kimoto, Kenneth N. Fish, and David A. Lewis, “Lower Glutamic Acid Decarboxylase 65-kDa Isoform Messenger RNA and Protein Levels in the Prefrontal Cortex in Schizoaffective Disorder but Not Schizophrenia,” Biological Psychiatry, 2014. View at Publisher · View at Google Scholar
  • Khaled Al Awam, Ida Sibylle Haußleiter, Ed Dudley, Rossen Donev, Martin Brüne, Georg Juckel, and Johannes Thome, “Multiplatform metabolome and proteome profiling identifies serum metabolite and protein signatures as prospective biomarkers for schizophrenia,” Journal of Neural Transmission, vol. 122, no. S1, pp. 111–122, 2014. View at Publisher · View at Google Scholar
  • Gabriele Deidda, Ignacio F. Bozarth, and Laura Cancedda, “Modulation of GABAergic transmission in development and neurodevelopmental disorders: investigating physiology and pathology to gain therapeutic perspectives,” Frontiers in Cellular Neuroscience, vol. 8, 2014. View at Publisher · View at Google Scholar
  • A. Eisen, M. Kiernan, H. Mitsumoto, and M. Swash, “Amyotrophic lateral sclerosis: a long preclinical period?,” Journal of Neurology, Neurosurgery & Psychiatry, vol. 85, no. 11, pp. 1232–1238, 2014. View at Publisher · View at Google Scholar
  • T Uchida, T Furukawa, S Iwata, Y Yanagawa, and A Fukuda, “Selective loss of parvalbumin-positive GABAergic interneurons in the cerebral cortex of maternally stressed Gad1-heterozygous mouse offspring,” Translational Psychiatry, vol. 4, no. 3, pp. e371, 2014. View at Publisher · View at Google Scholar
  • Chi-Ming A. Chen, Arielle D. Stanford, Xiangling Mao, Anissa Abi-Dargham, Dikoma C. Shungu, Sarah H. Lisanby, Charles E. Schroeder, and Lawrence S. Kegeles, “GABA level, gamma oscillation, and working memory performance in schizophrenia,” NeuroImage: Clinical, 2014. View at Publisher · View at Google Scholar
  • M. Engel, P. Snikeris, A. Jenner, T. Karl, X.-F. Huang, and E. Frank, “Neuregulin 1 Prevents Phencyclidine-Induced Behavioral Impairments and Disruptions to GABAergic Signaling in Mice,” International Journal of Neuropsychopharmacology, 2014. View at Publisher · View at Google Scholar
  • Louie N. van de Lagemaat, Bonnie Nijhof, Daniëlle G. M. Bosch, Mahdokht Kohansal-Nodehi, Shivakumar Keerthikumar, and J. Alexander Heimel, “Age-related decreased inhibitory vs. excitatory gene expression in the adult autistic brain,” Frontiers in Neuroscience, vol. 8, 2014. View at Publisher · View at Google Scholar
  • Robin Nguyen, Mark D. Morrissey, Vivek Mahadevan, Janine D. Cajanding, Melanie A. Woodin, John S. Yeomans, Kaori Takehara-Nishiuchi, and Jun Chul Kim, “Parvalbumin and GAD65 Interneuron Inhibition in the Ventral Hippocampus Induces Distinct Behavioral Deficits Relevant to Schizophrenia,” Journal of Neuroscience, vol. 34, no. 45, pp. 14948–14960, 2014. View at Publisher · View at Google Scholar
  • S. Hossein Fatemi, and Timothy D. Folsom, “GABA receptor subunit distribution and FMRP–mGluR5 signaling abnormalities in the cerebellum of subjects with schizophrenia, mood disorders, and autism,” Schizophrenia Research, 2014. View at Publisher · View at Google Scholar
  • Jessica Deslauriers, and Sylvain Grignon, “The Impact of Oxidative Stress on GAD67 Levels and Parvalbumin-Positive Neurons,” Studies on Psychiatric Disorders, pp. 451–467, 2014. View at Publisher · View at Google Scholar
  • Jonathan C. Bean, Thiri W. Lin, Anupama Sathyamurthy, Fang Liu, Dong-Min Yin, Wen-Cheng Xiong, and Lin Mei, “Genetic Labeling Reveals Novel Cellular Targets of Schizophrenia Susceptibility Gene: Distribution of GABA and Non-GABA ErbB4-Positive Cells in Adult Mouse Brain,” Journal of Neuroscience, vol. 34, no. 40, pp. 13549–13566, 2014. View at Publisher · View at Google Scholar
  • Michael P. Demars, and Hirofumi Morishita, “Cortical parvalbumin and somatostatin GABA neurons express distinct endogenous modulators of nicotinic acetylcholine receptors,” Molecular Brain, vol. 7, 2014. View at Publisher · View at Google Scholar
  • Mehran Mortazavi, Davood Farzin, Mehran Zarhghami, Seyed Hamzeh Hosseini, Parisa Mansoori, and Gholamreza Nateghi, “Efficacy of Zinc Sulfate as an Add-on Therapy to Risperidone Versus Risperidone Alone in Patients With Schizophrenia: A Double-Blind Randomized Placebo-Controlled Trial,” Iranian Journal of Psychiatry and Behavioral Sciences, vol. 9, no. 3, 2015. View at Publisher · View at Google Scholar
  • Stephan F. Taylor, and Ivy F. Tso, “GABA abnormalities in schizophrenia: A methodological review of in vivo studies,” Schizophrenia Research, vol. 167, no. 1-3, pp. 84–90, 2015. View at Publisher · View at Google Scholar
  • Tiziana Rubino, and Daniela Parolaro, “The Impact of Exposure to Cannabinoids in Adolescence: Insights from Animal Models,” Biological Psychiatry, 2015. View at Publisher · View at Google Scholar
  • T M Mueller, C E Remedies, V Haroutunian, and J H Meador-Woodruff, “Abnormal subcellular localization of GABAA receptor subunits in schizophrenia brain,” Translational Psychiatry, vol. 5, no. 8, pp. e612, 2015. View at Publisher · View at Google Scholar
  • Bao Hua Zhang, Mei Han, Xiang Yang Zhang, Li Hui, Shu Rong Jiang, Fu De Yang, Yun Long Tan, Zhi Ren Wang, Juan Li, and Xu Feng Huang, “Gender differences in cognitive deficits in schizophrenia with and without diabetes,” Comprehensive Psychiatry, 2015. View at Publisher · View at Google Scholar
  • Joseph A. McQuail, Charles J. Frazier, and Jennifer L. Bizon, “Molecular aspects of age-related cognitive decline: the role of GABA signaling,” Trends In Molecular Medicine, vol. 21, no. 7, pp. 450–460, 2015. View at Publisher · View at Google Scholar
  • J Smucny, K E Stevens, A Olincy, and J R Tregellas, “Translational utility of rodent hippocampal auditory gating in schizophrenia research: a review and evaluation,” Translational Psychiatry, vol. 5, no. 6, pp. e587, 2015. View at Publisher · View at Google Scholar
  • Mehran Mortazavi, Davood Farzin, Mehran Zarhghami, Seyed Hamzeh Hosseini, Parisa Mansoori, and Gholamreza Nateghi, “Efficacy of Zinc Sulfate as an Add-on Therapy to Risperidone versus Risperidone Alone in Patients With Schizophrenia: A Double-Blind Randomized Placebo-Controlled Trial,” Iranian Journal of Psychiatry and Behavioral Sciences, vol. 9, no. 1, 2015. View at Publisher · View at Google Scholar
  • Henry Silver, Nina Mandiuk, Reef Einoch, Ehud Susser, Lena Danovich, Warren Bilker, Moussa Youdim, and Orly Weinreb, “Improvement in verbal memory following SSRI augmentation of antipsychotic treatment is associated with changes in the expression of mRNA encoding for ,” International Clinical Psychopharmacology, vol. 30, no. 3, pp. 158–166, 2015. View at Publisher · View at Google Scholar
  • Kate E. Hoy, Neil W. Bailey, Sara L. Arnold, and Paul B. Fitzgerald, “The effect of transcranial Direct Current Stimulation on gamma activity and working memory in schizophrenia,” Psychiatry Research, 2015. View at Publisher · View at Google Scholar
  • Veronica Reinhart, Susan E. Bove, Dmitri Volfson, David A. Lewis, Robin J. Kleiman, and Thomas A. Lanz, “Evaluation of TrkB and BDNF transcripts in prefrontal cortex, hippocampus, and striatum from subjects with schizophrenia, bipolar disorder, and major ,” Neurobiology Of Disease, vol. 77, pp. 220–227, 2015. View at Publisher · View at Google Scholar
  • Hirofumi Morishita, Marija Kundakovic, Lucy Bicks, Amanda Mitchell, and Schahram Akbarian, “Interneuron epigenomes during the critical period of cortical plasticity: Implications for schizophrenia,” Neurobiology of Learning and Memory, 2015. View at Publisher · View at Google Scholar
  • Thomas A. Lanz, J. Julie Joshi, Veronica Reinhart, Kjell Johnson, Lonnie E. Grantham, and Dmitri Volfson, “STEP Levels Are Unchanged in Pre-Frontal Cortex and Associative Striatum in Post-Mortem Human Brain Samples from Subjects with Schizophrenia, Bipolar ,” Plos One, vol. 10, no. 3, 2015. View at Publisher · View at Google Scholar
  • Angela Vandenberg, David J. Piekarski, Natalia Caporale, Francisco Javier Munoz-Cuevas, and Linda Wilbrecht, “Adolescent maturation of inhibitory inputs onto cingulate cortex neurons is cell-type specific and TrkB dependent,” Frontiers in Neural Circuits, vol. 9, 2015. View at Publisher · View at Google Scholar
  • Amit Etkin, and Christopher Pittenger, “Are There Biological Commonalities Among Different Psychiatric Disorders?,” Psychiatry, pp. 243–257, 2015. View at Publisher · View at Google Scholar
  • Joanna M. Wierońska, Stevin H. Zorn, Dario Doller, and Andrzej Pilc, “Metabotropic glutamate receptors as targets for new antipsychotic drugs: Historical perspective and critical comparative assessment,” Pharmacology & Therapeutics, 2015. View at Publisher · View at Google Scholar
  • Patrick T. Piantadosi, Shahin Khayambashi, Magdalen G. Schluter, Agnes Kutarna, and Stan B. Floresco, “Perturbations in reward-related decision-making induced by reduced prefrontal cortical GABA transmission: Relevance for psychiatric disorders,” Neuropharmacology, 2015. View at Publisher · View at Google Scholar
  • Danielle John, and Darwin K. Berg, “Long-lasting changes in neural networks to compensate for altered nicotinic input,” Biochemical Pharmacology, vol. 97, no. 4, pp. 418–424, 2015. View at Publisher · View at Google Scholar
  • Andrea Lobo, and Teresa Summaviellepp. 148–176, 2015. View at Publisher · View at Google Scholar
  • J. Richetto, M. A. Labouesse, M. M. Poe, J. M. Cook, A. A. Grace, M. A. Riva, and U. Meyer, “Behavioral Effects of the Benzodiazepine-Positive Allosteric Modulator SH-053-2'F-S-CH3 in an Immune-Mediated Neurodevelopmental Disruption Model,” International Journal of Neuropsychopharmacology, vol. 18, no. 4, pp. pyu055–pyu055, 2015. View at Publisher · View at Google Scholar
  • Therese Riedemann, Christoph Schmitz, and Bernd Sutor, “Immunocytochemical heterogeneity of somatostatin-expressing GABAergic interneurons in layers II and III of the mouse cingulate cortex: A combined immunofluorescence/design-based stereologic study,” Journal of Comparative Neurology, vol. 524, no. 11, pp. 2281–2299, 2016. View at Publisher · View at Google Scholar
  • Alessia Luoni, Peter Gass, Paolo Brambilla, Mirella Ruggeri, Marco A. Riva, and Dragos Inta, “Altered expression of schizophrenia-related genes in mice lacking mGlu5 receptors,” European Archives of Psychiatry and Clinical Neuroscience, 2016. View at Publisher · View at Google Scholar
  • Akshat Gupta, Scott M. Barb, Summer A.F. Glass, Ilan Dinstein, Nancy J. Minshew, David J. Heeger, Shaun M. Eack, Marlene Behrmann, and Sarah M. Haigh, “Differential sensory fMRI signatures in autism and schizophrenia: Analysis of amplitude and trial-to-trial variability,” Schizophrenia Research, vol. 175, no. 1-3, pp. 12–19, 2016. View at Publisher · View at Google Scholar
  • Masoumeh Nozari, Toshimitsu Suzuki, Marcello G. P. Rosa, Kazuhiro Yamakawa, and Nafiseh Atapour, “The impact of early environmental interventions on structural plasticity of the axon initial segment in neocortex,” Developmental Psychobiology, vol. 59, no. 1, pp. 39–47, 2016. View at Publisher · View at Google Scholar
  • S. Kang, K. Paul, E. R. Hankosky, C. L. Cox, and J. M. Gulley, “D-1 Receptor-Mediated Inhibition Of Medial Prefrontal Cortex Neurons Is Disrupted In Adult Rats Exposed To Amphetamine In Adolescence,” Neuroscience, vol. 324, pp. 40–49, 2016. View at Publisher · View at Google Scholar
  • Enni Markkanen, Urs Meyer, and Grigory Dianov, “DNA Damage and Repair in Schizophrenia and Autism: Implications for Cancer Comorbidity and Beyond,” International Journal of Molecular Sciences, vol. 17, no. 6, pp. 856, 2016. View at Publisher · View at Google Scholar
  • Francesco Papaleo, Feng Yang, Clare Paterson, Sara Palumbo, Gregory V. Carr, Yanhong Wang, Kirsten Floyd, Wenwei Huang, Craig J. Thomas, Jingshan Chen, Daniel R. Weinberger, and Amanda J. Law, “Behavioral, Neurophysiological, and Synaptic Impairment in a Transgenic Neuregulin1 (NRG1-IV) Murine Schizophrenia Model,” Journal Of Neuroscience, vol. 36, no. 17, pp. 4859–4875, 2016. View at Publisher · View at Google Scholar
  • Kate E. Hoy, Dean Whitty, Neil Bailey, and Paul B. Fitzgerald, “Preliminary investigation of the effects of γ-tACS on working memory in schizophrenia,” Journal of Neural Transmission, vol. 123, no. 10, pp. 1205–1212, 2016. View at Publisher · View at Google Scholar
  • Aron T. Hill, Nigel C. Rogasch, Paul B. Fitzgerald, and Kate E. Hoy, “TMS-EEG: A window into the neurophysiological effects of transcranial electrical stimulation in non-motor brain regions,” Neuroscience & Biobehavioral Reviews, 2016. View at Publisher · View at Google Scholar
  • Ji-Tao Li, Yun-Ai Su, Hong-Li Wang, Ying-Ying Zhao, Xue-Mei Liao, Xiao-Dong Wang, and Tian-Mei Si, “Repeated Blockade of NMDA Receptors During Adolescence Impairs Reversal Learning and Disrupts GABAergic Interneurons in Rat Medial Prefrontal Cortex,” Frontiers in Molecular Neuroscience, vol. 9, 2016. View at Publisher · View at Google Scholar
  • Jianmin Su, Jiang Chen, Kumiko Lippold, Aboozar Monavarfeshani, Gabriela Lizana Carrillo, Rachel Jenkins, and Michael A. Fox, “Collagen-derived matricryptins promote inhibitory nerve terminal formation in the developing neocortex,” The Journal of Cell Biology, vol. 212, no. 6, pp. 721–736, 2016. View at Publisher · View at Google Scholar
  • Tong-Ju Li, Yang Zhao, Guo-Ming Dong, Bai-Ping Ma, and De-Xian Jia, “Gut microbiota and Alzheimer’s disease,” Journal of International Pharmaceutical Research, vol. 43, no. 1, pp. 15–19, 2016. View at Publisher · View at Google Scholar
  • Marco Fuenzalida, Claudia Espinoza, Miguel Angel Perez, Cheril Tapia-Rojas, Loreto Cuitino, Enrique Brandan, and Nibaldo C. Inestrosa, “Wnt signaling pathway improves central inhibitory synaptic transmission in a mouse model of Duchenne muscular dystrophy,” Neurobiology Of Disease, vol. 86, pp. 109–120, 2016. View at Publisher · View at Google Scholar
  • S Canetta, S Bolkan, N Padilla-Coreano, L J Song, R Sahn, N L Harrison, J A Gordon, A Brown, and C Kellendonk, “Maternal immune activation leads to selective functional deficits in offspring parvalbumin interneurons,” Molecular Psychiatry, 2016. View at Publisher · View at Google Scholar
  • Vicente Molina, Alejandro Bachiller, Vanessa Suazo, Alba Lubeiro, Jesus Poza, and Roberto Hornero, “Noise power associated with decreased task-induced variability of brain electrical activity in schizophrenia,” European Archives Of Psychiatry And Clinical Neuroscience, vol. 266, no. 1, pp. 55–61, 2016. View at Publisher · View at Google Scholar
  • Subhash C. Gupta, Aparna Ravikrishnan, Jinxu Liu, Zhihao Mao, Ratnamala Pavuluri, Brandon G. Hillman, Pauravi J. Gandhi, Dustin J. Stairs, Ming Li, Rajesh R. Ugale, Daniel T. Monaghan, and Shashank M. Dravid, “The NMDA receptor GluN2C subunit controls cortical excitatory-inhibitory balance, neuronal oscillations and cognitive function,” Scientific Reports, vol. 6, pp. 38321, 2016. View at Publisher · View at Google Scholar
  • Jiang, Zhang, Zhao, Wang, and Lin, “DNA methylation regulates gabrb2 mRNA expression: developmental variations and disruptions in l-methionine-induced zebrafish with schizophrenia-like symptoms,” Genes, Brain and Behavior, vol. 15, no. 8, pp. 702–710, 2016. View at Publisher · View at Google Scholar
  • Osamu Hoshino, Meihong Zheng, and Kazuo Watanabe, “Reduction of Trial-to-Trial Perceptual Variability by Intracortical Tonic Inhibition,” Neural Computation, vol. 28, no. 1, pp. 187–215, 2016. View at Publisher · View at Google Scholar
  • Nuwan C. Hettige, Gustavo H. F. de Moraes, James L. Kennedy, and Vincenzo De Luca, “Candidate gene analysis of pharmacodynamic targets for antipsychotic dosage,” Pharmacogenomics, vol. 17, no. 3, pp. 199–208, 2016. View at Publisher · View at Google Scholar
  • K.M. Friel, A.M. Gordon, J.B. Carmel, A. Kirton, and B.T. Gillick, “Pediatric Issues in Neuromodulation,” Pediatric Brain Stimulation, pp. 131–149, 2016. View at Publisher · View at Google Scholar
  • Hagar Tadmor, Idit Golani, Ravid Doron, Ilana Kremer, and Alon Shamir, “ErbB signaling antagonist ameliorates behavioral deficit induced by phencyclidine (PCP) in mice, without affecting metabolic syndrome markers,” Progress in Neuro-Psychopharmacology and Biological Psychiatry, 2017. View at Publisher · View at Google Scholar
  • Jeroen C. de Jonge, Christiaan H. Vinkers, Hilleke E. Hulshoff Pol, and Anouk Marsman, “GABAergic Mechanisms in Schizophrenia: Linking Postmortem and In Vivo Studies,” Frontiers in Psychiatry, vol. 8, 2017. View at Publisher · View at Google Scholar
  • Dionysios Xenos, Marija Kamceva, Simone Tomasi, Jessica A Cardin, Michael L Schwartz, and Flora M Vaccarino, “Loss of TrkB Signaling in Parvalbumin-Expressing Basket Cells Results in Network Activity Disruption and Abnormal Behavior,” Cerebral Cortex, vol. 28, no. 10, pp. 3399–3413, 2017. View at Publisher · View at Google Scholar
  • Shabeesh Balan, Kazuo Yamada, Yoshimi Iwayama, Takanori Hashimoto, Tomoko Toyota, Chie Shimamoto, Motoko Maekawa, Shu Takagai, Tomoyasu Wakuda, Yosuke Kameno, Daisuke Kurita, Kohei Yamada, Mitsuru Kikuchi, Tasuku Hashimoto, Nobuhisa Kanahara, and Takeo Yoshikawa, “Comprehensive association analysis of 27 genes from the GABAergic system in Japanese individuals affected with schizophrenia,” Schizophrenia Research, vol. 185, pp. 33–40, 2017. View at Publisher · View at Google Scholar
  • Yu-Chu Ella Chung, Shao-Chien Chen, Li-Chung Chuang, Wei-Liang Shih, Yi-Hang Chiu, Mong-Liang Lu, Hsi-Chung Chen, and Po-Hsiu Kuo, “Evaluation of the interaction between genetic variants of GAD1 and miRNA in bipolar disorders,” Journal of Affective Disorders, 2017. View at Publisher · View at Google Scholar
  • Anna-Maria Katsarou, Solomon L. Mosh?, and Aristea S. Galanopoulou, “Interneuronopathies and their role in early life epilepsies and neurodevelopmental disorders,” Epilepsia Open, 2017. View at Publisher · View at Google Scholar
  • Jantzen C. Collette, Lisha Choubey, and Karen Müller Smith, “­Glial and stem cell expression of murine Fibroblast Growth Factor Receptor 1 in the embryonic and perinatal nervous system,” PeerJ, vol. 5, pp. e3519, 2017. View at Publisher · View at Google Scholar
  • Kit Melissa Larsen, Giovanni Pellegrino, Michelle Rosgaard Birknow, Trine Nørgaard Kjær, William Frans Christiaan Baaré, Michael Didriksen, Line Olsen, Thomas Werge, Morten Mørup, and Hartwig Roman Siebner, “22q11.2 Deletion Syndrome Is Associated With Impaired Auditory Steady-State Gamma Response,” Schizophrenia Bulletin, vol. 44, no. 2, pp. 388–397, 2017. View at Publisher · View at Google Scholar
  • Lisha Choubey, Jantzen C. Collette, and Karen Müller Smith, “Quantitative assessment of fibroblast growth factor receptor 1 expression in neurons and glia,” PeerJ, vol. 5, pp. e3173, 2017. View at Publisher · View at Google Scholar
  • Javad Mirnajafi-Zadeh, Nafiseh Atapour, Amir Shojaei, and Afsaneh Kamali Anaraki, “Modifications of inhibitory transmission onto pyramidal neurons by postnatal exposure to MK-801: Effects of enriched environment,” International Journal of Developmental Neuroscience, vol. 57, pp. 56–61, 2017. View at Publisher · View at Google Scholar
  • Brian L. Allman, Nagalingam Rajakumar, and Sagar J. Desai, “Combination of behaviorally sub-effective doses of glutamate NMDA and dopamine D1 receptor antagonists impairs executive function,” Behavioural Brain Research, vol. 323, pp. 24–31, 2017. View at Publisher · View at Google Scholar
  • B.S. Beas, J.A. McQuail, C. Bañuelos, B. Setlow, and J.L. Bizon, “Prefrontal cortical GABAergic signaling and impaired behavioral flexibility in aged F344 rats,” Neuroscience, vol. 345, pp. 274–286, 2017. View at Publisher · View at Google Scholar
  • Yuki Imoto, Eri Segi-Nishida, Hidenori Suzuki, and Katsunori Kobayashi, “Rapid and stable changes in maturation-related phenotypes of the adult hippocampal neurons by electroconvulsive treatment,” Molecular Brain, vol. 10, no. 1, 2017. View at Publisher · View at Google Scholar
  • Yildiz Zengin-Toktas, and Sarah Cushing Woolley, “Singing modulates parvalbumin interneurons throughout songbird forebrain vocal control circuitry,” Plos One, vol. 12, no. 2, pp. e0172944, 2017. View at Publisher · View at Google Scholar
  • Jianmin Su, James Cole, and Michael A. Fox, “Loss of Interneuron-Derived Collagen XIX Leads to a Reduction in Perineuronal Nets in the Mammalian Telencephalon,” ASN Neuro, vol. 9, no. 1, pp. 175909141668902, 2017. View at Publisher · View at Google Scholar
  • M Lee, P Sehatpour, M J Hoptman, P Lakatos, E C Dias, J T Kantrowitz, A M Martinez, and D C Javitt, “Neural mechanisms of mismatch negativity dysfunction in schizophrenia,” Molecular Psychiatry, 2017. View at Publisher · View at Google Scholar
  • Kazu Nakazawa, Vivek Jeevakumar, and Kazuhito Nakao, “Spatial and temporal boundaries of NMDA receptor hypofunction leading to schizophrenia,” npj Schizophrenia, vol. 3, no. 1, 2017. View at Publisher · View at Google Scholar
  • Yi Liu, Xue-fei Sun, Mei Ding, Yong-ping Liu, Xi-cen Zhang, Hao Pang, Jia-xin Xing, Jin-feng Xuan, Xi Xia, Bao-jie Wang, and Jun Yao, “The GABRB3 Polymorphism and its Association with Schizophrenia,” Journal of Molecular Neuroscience, 2017. View at Publisher · View at Google Scholar
  • Ion R. Popescu, Kathy Q. Le, Rocío Palenzuela, Rebecca Voglewede, and Ricardo Mostany, “Marked bias towards spontaneous synaptic inhibition distinguishes non-adapting from adapting layer 5 pyramidal neurons in the barrel cortex,” Scientific Reports, 2017. View at Publisher · View at Google Scholar
  • Guanmei Cao, Richard A. E. Edden, Fei Gao, Hao Li, Tao Gong, Weibo Chen, Xiaohui Liu, Guangbin Wang, and Bin Zhao, “Reduced GABA levels correlate with cognitive impairment in patients with relapsing-remitting multiple sclerosis,” European Radiology, 2017. View at Publisher · View at Google Scholar
  • Maedbh King, “Gaba,” Encyclopedia of Personality and Individual Differences, pp. 1–3, 2017. View at Publisher · View at Google Scholar
  • Anna Schroeder, Matthew Hudson, Xin Du, Yee Wen, Candace Wu, Jay Nakamura, Maarten van den Buuse, Nigel C. Jones, and Rachel A. Hill, “Estradiol and raloxifene modulate hippocampal gamma oscillations during a spatial memory task,” Psychoneuroendocrinology, 2017. View at Publisher · View at Google Scholar
  • Murat ?lhan Atag?n, Elif Muazzez ??ko?lu, ?a?lar Soykan, Can Serdar S?leyman, Semra Ulusoy-Kaymak, Ali ?ayk?yl?, Oktay Alg?n, Mary Louise Phillips, Dost ?ng?r, and Constance Mary Moore, “Perisylvian GABA levels in schizophrenia and bipolar disorder,” Neuroscience Letters, vol. 637, pp. 70–74, 2017. View at Publisher · View at Google Scholar
  • Jan D. Andersson, David Matuskey, and Sjoerd J. Finnema, “Positron emission tomography imaging of the γ-aminobutyric acid system,” Neuroscience Letters, 2018. View at Publisher · View at Google Scholar
  • Justine Renard, Walter J. Rushlow, and Steven R. Laviolette, “Effects of Adolescent THC Exposure on the Prefrontal GABAergic System: Implications for Schizophrenia-Related Psychopathology,” Frontiers in Psychiatry, vol. 9, 2018. View at Publisher · View at Google Scholar
  • Candace Jones, “Impact of the Alpha-7 Nicotinic Acetylcholine Receptor on Long-Term Potentiation within the Hippocampus: Implications in Schizophrenia,” Psychiatric Annals, vol. 47, no. 7, pp. 345–348, 2018. View at Publisher · View at Google Scholar
  • Luisa A. Hasam-Henderson, Grace C. Gotti, Michele Mishto, Constantin Klisch, Zoltan Gerevich, Jörg R. P. Geiger, and Richard Kovács, “NMDA-receptor inhibition and oxidative stress during hippocampal maturation differentially alter parvalbumin expression and gamma-band activity,” Scientific Reports, vol. 8, no. 1, 2018. View at Publisher · View at Google Scholar
  • Negah Rahmati, Freek E. Hoebeek, Saša Peter, and Chris I. De Zeeuw, “Chloride Homeostasis in Neurons With Special Emphasis on the Olivocerebellar System: Differential Roles for Transporters and Channels,” Frontiers in Cellular Neuroscience, vol. 12, 2018. View at Publisher · View at Google Scholar
  • Javier Gomez-Pilar, Rodrigo de Luis-García, Alba Lubeiro, Henar de la Red, Jesús Poza, Pablo Núñez, Roberto Hornero, and Vicente Molina, “Relations between structural and EEG-based graph metrics in healthy controls and schizophrenia patients,” Human Brain Mapping, 2018. View at Publisher · View at Google Scholar
  • Emily R. Hankosky, Sara R. Westbrook, Rachel M. Haake, Jari Willing, Lori T. Raetzman, Janice M. Juraska, and Joshua M. Gulley, “Age- and sex-dependent effects of methamphetamine on cognitive flexibility and 5-HT 2C receptor localization in the orbitofrontal cortex of Sprague-Dawley rats,” Behavioural Brain Research, 2018. View at Publisher · View at Google Scholar
  • Karen Müller Smith, “Hyperactivity in mice lacking one allele of the glutamic acid decarboxylase 67 gene,” ADHD Attention Deficit and Hyperactivity Disorders, 2018. View at Publisher · View at Google Scholar
  • Mohammadreza Moradi, Massoud Saidijam, Reza Yadegarazari, Leila Jahangard, Maryam Seifi, Nasrin Matinnia, and Ali Ghaleiha, “Genes Encoding GABA-β and HT1D Receptors in Bipolar I (Manic Phase) Patients,” Basic and Clinical Neuroscience Journal, vol. 9, no. 2, pp. 129–134, 2018. View at Publisher · View at Google Scholar
  • Tao Tan, Wei Wang, Jamal Williams, Kaijie Ma, Qing Cao, and Zhen Yan, “Stress Exposure in Dopamine D4 Receptor Knockout Mice Induces Schizophrenia-Like Behaviors via Disruption of GABAergic Transmission,” Schizophrenia Bulletin, 2018. View at Publisher · View at Google Scholar
  • Alexander G Murley, and James B Rowe, “Neurotransmitter deficits from frontotemporal lobar degeneration,” Brain, vol. 141, no. 5, pp. 1263–1285, 2018. View at Publisher · View at Google Scholar
  • Osamu Hoshino, Meihong Zheng, and Kazuo Watanabe, “Perceptual judgments via sensory-motor interaction assisted by cortical GABA,” Journal of Computational Neuroscience, 2018. View at Publisher · View at Google Scholar
  • Joseph A. McQuail, Sarah A. Johnson, Sara N. Burke, and Jennifer L. Bizon, “Rat Models of Cognitive Aging,” Conn's Handbook of Models for Human Aging, pp. 211–230, 2018. View at Publisher · View at Google Scholar
  • Ryan J. Duchatel, Cynthia Shannon Weickert, and Paul A. Tooney, “White matter neuron biology and neuropathology in schizophrenia,” npj Schizophrenia, vol. 5, no. 1, 2019. View at Publisher · View at Google Scholar
  • H Trantham-Davidson, and A Lavin, “Loss of dysbindin-1 affects GABAergic transmission in the PFC,” Psychopharmacology, 2019. View at Publisher · View at Google Scholar
  • Thomas A. Lanz, Veronica Reinhart, Mark J. Sheehan, Stacey J. Sukoff Rizzo, Susan E. Bove, Larry C. James, Dmitri Volfson, David A. Lewis, and Robin J. Kleiman, “Postmortem transcriptional profiling reveals widespread increase in inflammation in schizophrenia: a comparison of prefrontal cortex, striatum, and hippocampus among matched tetrads of controls with subjects diagnosed with schizophrenia, bipolar or major depressive disorder,” Translational Psychiatry, vol. 9, no. 1, 2019. View at Publisher · View at Google Scholar
  • Sara de la Salle, Dhrasti Shah, Joelle Choueiry, Hayley Bowers, Judy McIntosh, Vadim Ilivitsky, and Verner Knott, “NMDA Receptor Antagonist Effects on Speech-Related Mismatch Negativity and Its Underlying Oscillatory and Source Activity in Healthy Humans,” Frontiers in Pharmacology, vol. 10, 2019. View at Publisher · View at Google Scholar
  • F. Piras, F. Piras, N. Banaj, V. Ciullo, D. Vecchio, R. A. E. Edden, and G. Spalletta, “Cerebellar GABAergic correlates of cognition‐mediated verbal fluency in physiology and schizophrenia,” Acta Psychiatrica Scandinavica, 2019. View at Publisher · View at Google Scholar
  • Elisa Capecci, Nikola Kasabov, and Josafath I. Espinosa-Ramos, “A Computational Model of Neuroreceptor-Dependent Plasticity (NRDP) Based on Spiking Neural Networks,” IEEE Transactions on Cognitive and Developmental Systems, vol. 11, no. 1, pp. 63–72, 2019. View at Publisher · View at Google Scholar
  • Hiroshi Ueno, Kazuki Fujii, Keizo Takao, Shunsuke Suemitsu, Shinji Murakami, Naoya Kitamura, Kenta Wani, Yosuke Matsumoto, Motoi Okamoto, and Takeshi Ishihara, “Alteration of parvalbumin expression and perineuronal nets formation in the cerebral cortex of aged mice,” Molecular and Cellular Neuroscience, 2019. View at Publisher · View at Google Scholar