Cited by 322Autism Spectrum Disorder ResearchGenetics and Neurodevelopmental DisordersNeuroscience and Neuropharmacology Research

The DOI matches its Crossref record; 112 of the 113 references it cites were found in a registry or an index.

The Number of Parvalbumin-Expressing Interneurons Is Decreased in the Medial Prefrontal Cortex in Autism

Open access

Hashemi, Ezzat, Ariza, Jeanelle, Rogers, Haille, Noctor, Stephen C., Martínez-Cerdeño, Verónica·2016·Cerebral Cortex

DOI 10.1093/cercor/bhw021PMC PMC6074948

Open this paper in CoChat — free account Open PDF

Abstract

The cognitive phenotype of autism has been correlated with an altered balance of excitation to inhibition in the cerebral cortex, which could result from a change in the number, function, or morphology of GABA-expressing interneurons. The number of GABAergic interneuron subtypes has not been quantified in the autistic cerebral cortex. We classified interneurons into 3 subpopulations based on expression of the calcium-binding proteins parvalbumin, calbindin, or calretinin. We quantified the number of each interneuron subtype in postmortem neocortical tissue from 11 autistic cases and 10 control cases. Prefrontal Brodmann Areas (BA) BA46, BA47, and BA9 in autism and age-matched controls were analyzed by blinded researchers. We show that the number of parvalbumin+ interneurons in these 3 cortical areas-BA46, BA47, and BA9-is significantly reduced in autism compared with controls. The number of calbindin+ and calretinin+ interneurons did not differ in the cortical areas examined. Parvalbumin+ interneurons are fast-spiking cells that synchronize the activity of pyramidal cells through perisomatic and axo-axonic inhibition. The reduced number of parvalbumin+ interneurons could disrupt the balance of excitation/inhibition and alter gamma wave oscillations in the cerebral cortex of autistic subjects. These data will allow development of novel treatments specifically targeting parvalbumin interneurons.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Integrity signals

Registry

Crossref · 10.1093/cercor/bhw021

Cites

112 of 112 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Epigenetic Regulations of GABAergic Neurotransmission: Relevance for Neurological Disorders and Epigenetic Therapy
Shrestha, S., & Offer, S. M. (2016) · Medical Epigenetics · doi:10.1159/000444713 · Cited by 8,951
The origin of extracellular fields and currents — EEG, ECoG, LFP and spikes
Buzsáki, G., Anastassiou, C. A., & Koch, C. (2012) · Nature Reviews Neuroscience · doi:10.1038/nrn3241 · Cited by 4,225
Interneurons of the neocortical inhibitory system
Markram, H., Toledo-Rodriguez, M., Wang, Y., Gupta, A., Silberberg, G., & Wu, C. (2004) · Nature Reviews Neuroscience · doi:10.1038/nrn1519 · Cited by 2,954
Mechanisms of Gamma Oscillations
Buzsáki, G., & Wang, X.-J. (2012) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-062111-150444 · Cited by 2,796
Model of autism: increased ratio of excitation/inhibition in key neural systems
Rubenstein, J. L. R., & Merzenich, M. M. (2003) · Genes, Brain and Behavior · doi:10.1034/j.1601-183x.2003.00037.x · Cited by 2,768
Parvalbumin neurons and gamma rhythms enhance cortical circuit performance
Sohal, V. S., Zhang, F., Yizhar, O., & Deisseroth, K. (2009) · Nature · doi:10.1038/nature07991 · Cited by 2,606
Driving fast-spiking cells induces gamma rhythm and controls sensory responses
Cardin, J. A., Carlén, M., Meletis, K., Knoblich, U., Zhang, F., Deisseroth, K., Tsai, L.-H., & Moore, C. I. (2009) · Nature · doi:10.1038/nature08002 · Cited by 2,603
Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks
Bartos, M., Vida, I., & Jonas, P. (2007) · Nature Reviews Neuroscience · doi:10.1038/nrn2044 · Cited by 2,070
Prevalence of autism spectrum disorders--autism and developmental disabilities monitoring network, 14 sites, United States, 2002.
(2007) · PubMed · Cited by 2,018
Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation
Whittington, M. A., Traub, R. D., & Jefferys, J. G. R. (1995) · Nature · doi:10.1038/373612a0 · Cited by 1,613
GABAergic cell subtypes and their synaptic connections in rat frontal cortex
Kawaguchi, Y. (1997) · Cerebral Cortex · doi:10.1093/cercor/7.6.476 · Cited by 1,416
EEG evidence for mirror neuron dysfunction in autism spectrum disorders
Oberman, L. M., Hubbard, E. M., McCleery, J. P., Altschuler, E. L., Ramachandran, V. S., & Pineda, J. A. (2005) · Cognitive Brain Research · doi:10.1016/j.cogbrainres.2005.01.014 · Cited by 1,146 · cited 1×
“EEG recordings from the cerebral cortex of autistic patients exhibit an alteration of induced gamma activity patterns (Belmonte and Yurgelun-Todd 2003; Brown et al. 2005; Oberman et al. 2005; Orekhova et al. 2007; Cohen et al. 2009; Milne et al. 2009; Russo et al. 2009; Thatcher et al. 2009).”
Background
Cortical parvalbumin interneurons and cognitive dysfunction in schizophrenia
Lewis, D. A., Curley, A. A., Glausier, J. R., & Volk, D. W. (2012) · Trends in Neurosciences · doi:10.1016/j.tins.2011.10.004 · Cited by 1,071
A Neuroligin-3 Mutation Implicated in Autism Increases Inhibitory Synaptic Transmission in Mice
Tabuchi, K., Blundell, J., Etherton, M. R., Hammer, R. E., Liu, X., Powell, C. M., & Südhof, T. C. (2007) · Science · doi:10.1126/science.1146221 · Cited by 997
Prevalence of autism spectrum disorders--Autism and Developmental Disabilities Monitoring Network, 14 sites, United States, 2008.
(2012) · PubMed · Cited by 852
New insights into the classification and nomenclature of cortical GABAergic interneurons
DeFelipe, J., López-Cruz, P. L., Benavides-Piccione, R., Bielza, C., Larrañaga, P., Anderson, S., Burkhalter, A., Cauli, B., Fairén, A., Feldmeyer, D., et al. (2013) · Nature Reviews Neuroscience · doi:10.1038/nrn3444 · Cited by 833
Neuron Number and Size in Prefrontal Cortex of Children With Autism
Courchesne, E., Mouton, P. R., Calhoun, M. E., Semendeferi, K., Ahrens-Barbeau, C., Hallet, M. J., Barnes, C. C., & Pierce, K. (2011) · JAMA · doi:10.1001/jama.2011.1638 · Cited by 779
Molecular and Physiological Diversity of Cortical Nonpyramidal Cells
Cauli, B., Audinat, E., Lambolez, B., Angulo, M. C., Ropert, N., Tsuzuki, K., Hestrin, S., & Rossier, J. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-10-03894.1997 · Cited by 738
Reduced cortical activity due to a shift in the balance between excitation and inhibition in a mouse model of Rett Syndrome
Dani, V. S., Chang, Q., Maffei, A., Turrigiano, G. G., Jaenisch, R., & Nelson, S. B. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0506071102 · Cited by 639
Excitatory effect of GABAergic axo-axonic cells in cortical microcircuits
Szabadics, J., Varga, C., Molnár, G., Oláh, S., Barzó, P., & Tamás, G. (2006) · Science · doi:10.1126/science.1121325 · Cited by 598
GABA Neurons and the Mechanisms of Network Oscillations: Implications for Understanding Cortical Dysfunction in Schizophrenia
González‐Burgos, G., & Lewis, D. A. (2008) · Schizophrenia Bulletin · doi:10.1093/schbul/sbn070 · Cited by 592
Types of neurons, synaptic connections and chemical characteristics of cells immunoreactive for calbindin-D28K, parvalbumin and calretinin in the neocortex
DeFelipe, J. (1997) · Journal of Chemical Neuroanatomy · doi:10.1016/s0891-0618(97)10013-8 · Cited by 550
A specific ‘axo-axonal’ interneuron in the visual cortex of the rat
Somogyi, P. (1977) · Brain Research · doi:10.1016/0006-8993(77)90808-3 · Cited by 530
Conceptual Models of Neural Organization.
Pritchard, J. J. (1976) · Europe PMC (PubMed Central) · Cited by 514
Mice lacking Dlx1 show subtype-specific loss of interneurons, reduced inhibition and epilepsy
Cobos, I., Calcagnotto, M. E., Vilaythong, A. J., Thwin, M. T., Noebels, J. L., Baraban, S. C., & Rubenstein, J. L. R. (2005) · Nature Neuroscience · doi:10.1038/nn1499 · Cited by 502
Local circuit neurons immunoreactive for calretinin, calbindin D‐28k or parvalbumin in monkey prefronatal cortex: Distribution and morphology
Condé, F., Lund, J. S., Jacobowitz, D. M., Baimbridge, K. G., & Lewis, D. A. (1994) · The Journal of Comparative Neurology · doi:10.1002/cne.903410109 · Cited by 500
Neuron Number and Size in Prefrontal Cortex of Children With Autism
Stockman, J. A. (2012) · Yearbook of Pediatrics · doi:10.1016/j.yped.2011.12.022 · Cited by 491
Fast spiking cells in rat hippocampus (CA1 region) contain the calcium-binding protein parvalbumin
Kawaguchi, Y., Katsumaru, H., Kosaka, T., Heizmann, C. W., & Hama, K. (1987) · Brain Research · doi:10.1016/0006-8993(87)90921-8 · Cited by 485
Stereological Analysis of Amygdala Neuron Number in Autism
Schumann, C. M., & Amaral, D. G. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.1285-06.2006 · Cited by 413
Cellular distribution of the calcium-binding proteins parvalbumin, calbindin, and calretinin in the neocortex of mammals: phylogenetic and developmental patterns
Hof, P. R., Glezer, I. I., Condé, F., Flagg, R. A., Rubin, M. B., Nimchinsky, E. A., & Weisenhorn, D. M. V. (1999) · Journal of Chemical Neuroanatomy · doi:10.1016/s0891-0618(98)00065-9 · Cited by 411
A subclass of prefrontal γ-aminobutyric acid axon terminals are selectively altered in schizophrenia
Woo, T.-U. W., Whitehead, R. E., Melchitzky, D. S., & Lewis, D. A. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.9.5341 · Cited by 410
Role of the calcium-binding protein parvalbumin in short-term synaptic plasticity
Caillard, O., Moreno, H., Schwaller, B., Llano, I., Celio, M. R., & Marty, A. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.230362997 · Cited by 406
Anatomical, Physiological, Molecular and Circuit Properties of Nest Basket Cells in the Developing Somatosensory Cortex
Wang, Y. (2002) · Cerebral Cortex · doi:10.1093/cercor/12.4.395 · Cited by 382
Human prefrontal cortex
Teffer, K., & Semendeferi, K. (2012) · Progress in brain research · doi:10.1016/b978-0-444-53860-4.00009-x · Cited by 367
Three distinct subpopulations of GABAergic neurons in rat frontal agranular cortex
Kubota, Y., Hattori, R., & Yui, Y. (1994) · Brain Research · doi:10.1016/0006-8993(94)91060-x · Cited by 365
Purkinje Cell Size Is Reduced in Cerebellum of Patients with Autism
Fatemi, S. H., Halt, A. R., Realmuto, G., Earle, J., Kist, D. A., Thuras, P., & Merz, A. (2002) · Cellular and Molecular Neurobiology · doi:10.1023/a:1019861721160 · Cited by 344
Conceptual models of neural organization.
Szentágothai, J., & Arbib, M. A. (1974) · PubMed · Cited by 329
A novel network of multipolar bursting interneurons generates theta frequency oscillations in neocortex
Blatow, M., Rozov, A., Katona, I., Hormuzdi, S. G., Meyer, A. H., Whittington, M. A., Caputi, A., & Monyer, H. (2003) · Neuron · doi:10.1016/s0896-6273(03)00300-3 · Cited by 316
Altered neural connectivity in excitatory and inhibitory cortical circuits in autism
Zikopoulos, B., & Barbas, H. (2013) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2013.00609 · Cited by 313
GABAergic Depolarization of the Axon Initial Segment in Cortical Principal Neurons Is Caused by the Na–K–2Cl Cotransporter NKCC1
Khirug, S., Yamada, J., Afzalov, R., Voipio, J., Khiroug, L., & Kaila, K. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.0908-08.2008 · Cited by 304
Chandelier cells and epilepsy
DeFelipe, J. (1999) · Brain · doi:10.1093/brain/122.10.1807 · Cited by 297
Alterations in Chandelier Neuron Axon Terminals in the Prefrontal Cortex of Schizophrenic Subjects
Pierri, J. N., Chaudry, A. S., Woo, T.-U. W., & Lewis, D. A. (1999) · American Journal of Psychiatry · doi:10.1176/ajp.156.11.1709 · Cited by 294
Development of abstract thinking during childhood and adolescence: the role of rostrolateral prefrontal cortex
Dumontheil, I. (2014) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2014.07.009 · Cited by 293
Excess of High Frequency Electroencephalogram Oscillations in Boys with Autism
Orekhova, E. V., Stroganova, T. A., Nygren, G., Tsetlin, M. M., Posikera, I. N., Gillberg, C., & Elam, M. (2007) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.12.029 · Cited by 283
Annual Research Review: The role of the environment in the developmental psychopathology of autism spectrum condition
Mandy, W., & Lai, M. (2016) · Journal of Child Psychology and Psychiatry · doi:10.1111/jcpp.12501 · Cited by 283
K+ Channels at the Axon Initial Segment Dampen Near-Threshold Excitability of Neocortical Fast-Spiking GABAergic Interneurons
Goldberg, E. M., Clark, B. D., Zagha, E., Nahmani, M., Erisir, A., & Rudy, B. (2008) · Neuron · doi:10.1016/j.neuron.2008.03.003 · Cited by 271
Cerebellar Purkinje Cells are Reduced in a Subpopulation of Autistic Brains: A Stereological Experiment Using Calbindin-D28k
Whitney, E. R., Kemper, T. L., Bauman, M. L., Rosene, D. L., & Blatt, G. J. (2008) · The Cerebellum · doi:10.1007/s12311-008-0043-y · Cited by 268
Functional anatomy of impaired selective attention and compensatory processing in autism
Belmonte, M. K., & Yurgelun-Todd, D. A. (2003) · Cognitive Brain Research · doi:10.1016/s0926-6410(03)00189-7 · Cited by 266
Reciprocal Alterations in Pre- and Postsynaptic Inhibitory Markers at Chandelier Cell Inputs to Pyramidal Neurons in Schizophrenia
Volk, D. W. (2002) · Cerebral Cortex · doi:10.1093/cercor/12.10.1063 · Cited by 264
Neurons in the fusiform gyrus are fewer and smaller in autism
van Kooten, I. A. J., Palmen, S. J. M. C., von Cappeln, P., Steinbusch, H. W. M., Korr, H., Heinsen, H., Hof, P. R., van Engeland, H., & Schmitz, C. (2008) · Brain · doi:10.1093/brain/awn033 · Cited by 263
Lack of parvalbumin in mice leads to behavioral deficits relevant to all human autism core symptoms and related neural morphofunctional abnormalities
Wöhr, M., Orduz, D., Gregory, P., Moreno, H., Khan, U., Vörckel, K. J., Wolfer, D. P., Welzl, H., Gall, D., Schiffmann, S. N., et al. (2015) · Translational Psychiatry · doi:10.1038/tp.2015.19 · Cited by 258
Multiple origins of the cortical gamma rhythm
Whittington, M. A., Cunningham, M. O., LeBeau, F. E. N., Racca, C., & Traub, R. D. (2011) · Developmental Neurobiology · doi:10.1002/dneu.20814 · Cited by 253
Major defects in neocortical GABAergic inhibitory circuits in mice lacking the fragile X mental retardation protein
Selby, L., Zhang, C., & Sun, Q.-Q. (2007) · Neuroscience Letters · doi:10.1016/j.neulet.2006.11.062 · Cited by 245
Interneurons hyperpolarize pyramidal cells along their entire somatodendritic axis
Glickfeld, L. L., Roberts, J. D. B., Somogyi, P., & Scanziani, M. (2008) · Nature Neuroscience · doi:10.1038/nn.2230 · Cited by 238
Three hypotheses for developmental defects that may underlie some forms of autism spectrum disorder
Rubenstein, J. L. (2010) · Current Opinion in Neurology · doi:10.1097/wco.0b013e328336eb13 · Cited by 230
Variability in the terminations of GABAergic chandelier cell axons on initial segments of pyramidal cell axons in the monkey sensory‐motor cortex
DeFelipe, J., Hendry, S. H. C., Jones, E. G., & Schmechel, D. E. (1985) · The Journal of Comparative Neurology · doi:10.1002/cne.902310307 · Cited by 229
Toward a developmental neurobiology of autism
Polleux, F., & Lauder, J. M. (2004) · Mental Retardation and Developmental Disabilities Research Reviews · doi:10.1002/mrdd.20044 · Cited by 219
Association of the homeobox transcription factor, ENGRAILED 2, 3, with autism spectrum disorder
Gharani, N., Benayed, R., Mancuso, V., Brzustowicz, L. M., & Millonig, J. H. (2004) · Molecular Psychiatry · doi:10.1038/sj.mp.4001498 · Cited by 216
Clinical and Macroscopic Correlates of Minicolumnar Pathology in Autism
Casanova, M. F., Buxhoeveden, D. P., & Brown, C. (2002) · Journal of Child Neurology · doi:10.1177/088307380201700908 · Cited by 195
Association of DISC1 with autism and Asperger syndrome
Kilpinen, H., Ylisaukko‐oja, T., Hennah, W., Palo, O. M., Varilo, T., Vanhala, R., Wendt, T. N., von Wendt, L., Paunio, T., & Peltonen, L. (2007) · Molecular Psychiatry · doi:10.1038/sj.mp.4002031 · Cited by 193
Fragile X spectrum disorders
Lozano, R., Rosero, C. A., & Hagerman, R. J. (2014) · Intractable & Rare Diseases Research · doi:10.5582/irdr.2014.01022 · Cited by 186
Regional Alterations in Purkinje Cell Density in Patients with Autism
Skefos, J., Cummings, C., Enzer, K. G., Holiday, J., Weed, K., Levy, E., Yuce, T. K., Kemper, T. L., & Bauman, M. L. (2014) · PLoS ONE · doi:10.1371/journal.pone.0081255 · Cited by 181
The “Psychic” Neuron of the Cerebral Cortex
Goldman, P. S. (1999) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1999.tb11270.x · Cited by 178
Support for the Homeobox Transcription Factor Gene ENGRAILED 2 as an Autism Spectrum Disorder Susceptibility Locus
Benayed, R., Gharani, N., Rossman, I. T., Mancuso, V., Lazar, G., Kamdar, S., Bruse, S., Tischfield, S., Smith, B. J., Zimmerman, R., et al. (2005) · The American Journal of Human Genetics · doi:10.1086/497705 · Cited by 177
Representation and Integration of Auditory and Visual Stimuli in the Primate Ventral Lateral Prefrontal Cortex
Romanski, L. M. (2007) · Cerebral Cortex · doi:10.1093/cercor/bhm099 · Cited by 169
Development of rostral prefrontal cortex and cognitive and behavioural disorders
Dumontheil, I., Burgess, P. W., & Blakemore, S. (2008) · Developmental Medicine & Child Neurology · doi:10.1111/j.1469-8749.2008.02026.x · Cited by 168
The lateral prefrontal cortex and complex value-based learning and decision making
Dixon, M. L., & Kalina Christoff, A. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.04.011 · Cited by 167
Gamma abnormalities during perception of illusory figures in autism
Brown, C., Gruber, T., Boucher, J., Rippon, G., & Brock, J. (2005) · Cortex · doi:10.1016/s0010-9452(08)70273-9 · Cited by 166
Parvalbumin-, calbindin-, and calretinin-immunoreactive hippocampal interneuron density in autism
Lawrence, Y. A., Kemper, T. L., Bauman, M. L., & Blatt, G. J. (2009) · Acta Neurologica Scandinavica · doi:10.1111/j.1600-0404.2009.01234.x · Cited by 165
von Economo neurons in autism: A stereologic study of the frontoinsular cortex in children
Santos, M., Uppal, N., Butti, C., Wicinski, B., Schmeidler, J., Giannakopoulos, P., Heinsen, H., Schmitz, C., & Hof, P. R. (2011) · Brain Research · doi:10.1016/j.brainres.2010.08.067 · Cited by 164
Depolarizing effect of neocortical chandelier neurons
Woodruff, A. (2009) · Frontiers in Neural Circuits · doi:10.3389/neuro.04.015.2009 · Cited by 163
Impaired prefrontal inhibition in schizophrenia: relevance for cognitive dysfunction
Volk, D. W., & Lewis, D. A. (2002) · Physiology & Behavior · doi:10.1016/s0031-9384(02)00936-8 · Cited by 154
Stereological study of the neuronal number and volume of 38 brain subdivisions of subjects diagnosed with autism reveals significant alterations restricted to the striatum, amygdala and cerebellum
Węgiel, J., Flory, M. J., Kuchna, I., Nowicki, K., Ma, S. Y., Imaki, H., Wegiel, J., Cohen, I. L., London, E., Wısnıewskı, T., et al. (2014) · Acta Neuropathologica Communications · doi:10.1186/s40478-014-0141-7 · Cited by 153
Independent component analysis reveals atypical electroencephalographic activity during visual perception in individuals with autism
Milne, E., Scope, A., Pascalis, O., Buckley, D., & Makeig, S. (2009) · Biological Psychiatry · doi:10.1016/j.biopsych.2008.07.017 · Cited by 148
Altered parvalbumin basket cell inputs in the dorsolateral prefrontal cortex of schizophrenia subjects
Glausier, J. R., Fish, K. N., & Lewis, D. A. (2014) · Molecular Psychiatry · doi:10.1038/mp.2013.152 · Cited by 147
The autism‐epilepsy connection
Levisohn, P. M. (2007) · Epilepsia · doi:10.1111/j.1528-1167.2007.01399.x · Cited by 146
Synaptogenesis: A Balancing Act between Excitation and Inhibition
Cline, H. T. (2005) · Current Biology · doi:10.1016/j.cub.2005.03.010 · Cited by 146
Effects of Background Noise on Cortical Encoding of Speech in Autism Spectrum Disorders
Russo‐Ponsaran, N. M., Zecker, S. G., Trommer, B. L., Chen, J., & Kraus, N. (2009) · Journal of Autism and Developmental Disorders · doi:10.1007/s10803-009-0737-0 · Cited by 142
Density of cerebellar basket and stellate cells in autism: Evidence for a late developmental loss of Purkinje cells
Whitney, E. R., Kemper, T. L., Rosene, D. L., Bauman, M. L., & Blatt, G. J. (2009) · Journal of Neuroscience Research · doi:10.1002/jnr.22056 · Cited by 142
Depletion of MAP2 expression and laminar cytoarchitectonic changes in dorsolateral prefrontal cortex in adult autistic individuals
Mukaetova‐Ladinska, E. B., Arnold, H., Jaros, E., Perry, R., & Perry, E. (2004) · Neuropathology and Applied Neurobiology · doi:10.1111/j.1365-2990.2004.00574.x · Cited by 115
Loss of GABAergic neurons in the hippocampus and cerebral cortex of Engrailed-2 null mutant mice: Implications for autism spectrum disorders
Sgadó, P., Genovesi, S., Kalinovsky, A., Zunino, G., Macchi, F., Allegra, M., Murenu, E., Provenzano, G., Tripathi, P. P., Casarosa, S., et al. (2013) · Experimental Neurology · doi:10.1016/j.expneurol.2013.01.021 · Cited by 111
The Medial Prefrontal Cortex and Integration in Autism
Shalom, D. B. (2009) · The Neuroscientist · doi:10.1177/1073858409336371 · Cited by 106
Diversity and overlap of parvalbumin and somatostatin expressing interneurons in mouse presubiculum
Nassar, M., Simonnet, J., Lofredi, R., Cohen, I., Savary, E., Yanagawa, Y., Miles, R., & Fricker, D. (2015) · Frontiers in Neural Circuits · doi:10.3389/fncir.2015.00020 · Cited by 104
Stereological estimation of the number of neurons in the human amygdaloid complex
Schumann, C. M., & Amaral, D. G. (2005) · The Journal of Comparative Neurology · doi:10.1002/cne.20704 · Cited by 100
The Enigmatic Function of Chandelier Cells
Woodruff, A. R., Anderson, S. A., & Yuste, R. (2010) · Frontiers in Neuroscience · doi:10.3389/fnins.2010.00201 · Cited by 97
Hierarchical processing in the prefrontal cortex in a variety of cognitive domains
Jeon, H. (2014) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2014.00223 · Cited by 88
A Topographic Study of Minicolumnar Core Width by Lamina Comparison between Autistic Subjects and Controls: Possible Minicolumnar Disruption due to an Anatomical Element In‐Common to Multiple Laminae
Casanova, M. F., El-Baz, A. S., Vanbogaert, E., Narahari, P., & Switala, A. E. (2009) · Brain Pathology · doi:10.1111/j.1750-3639.2009.00319.x · Cited by 87
Imbalance of immunohistochemically characterized interneuron populations in the adolescent and adult rodent medial prefrontal cortex after repeated exposure to neonatal separation stress
Helmeke, C., Ovtscharoff, W. A., Poeggel, G., & Braun, K. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2007.12.023 · Cited by 77
Association of the ENGRAILED 2 (EN2) gene with autism in Chinese Han population
Wang, L., Jia, M., Yue, W., Tang, F., Qu, M., Ruan, Y., Lu, T., Zhang, H., Yan, H., Liu, J., et al. (2007) · American Journal of Medical Genetics Part B Neuropsychiatric Genetics · doi:10.1002/ajmg.b.30623 · Cited by 74
Clinical Genetic Aspects of Autism Spectrum Disorders
Schaefer, G. B. (2016) · International Journal of Molecular Sciences · doi:10.3390/ijms17020180 · Cited by 74
Colocalization of parvalbumin and calbindin D-28k in neurons including chandelier cells of the human temporal neocortex
del Rı́o, M. R., & DeFelipe, J. (1997) · Journal of Chemical Neuroanatomy · doi:10.1016/s0891-0618(96)00191-3 · Cited by 70
Relationships among Parvalbumin-Immunoreactive Neuron Density, Phase-Locked Gamma Oscillations, and Autistic/Schizophrenic Symptoms in PDGFR-β Knock-Out and Control Mice
Nakamura, T., Matsumoto, J., Takamura, Y., Ishii, Y., Sasahara, M., Ono, T., & Nishijo, H. (2015) · PLoS ONE · doi:10.1371/journal.pone.0119258 · Cited by 65
Autism and EEG Phase Reset: Deficient GABA Mediated Inhibition in Thalamo-Cortical Circuits
Thatcher, R. W., North, D. M., Neubrander, J. A., Biver, C. J., Cutler, S., & DeFina, P. A. (2009) · Developmental Neuropsychology · doi:10.1080/87565640903265178 · Cited by 64
Prenatal Exposure to Autism-Specific Maternal Autoantibodies Alters Proliferation of Cortical Neural Precursor Cells, Enlarges Brain, and Increases Neuronal Size in Adult Animals
Martínez-Cerdeño, V., Camacho, J., Fox, E., Miller, E., Ariza, J., Kienzle, D., Plank, K., Noctor, S. C., & Van de Water, J. (2016) · Cerebral Cortex · doi:10.1093/cercor/bhu291 · Cited by 63
Self-citation
A 1q42 deletion involving DISC1, DISC2, and TSNAX in an autism spectrum disorder
Williams, J. M., Beck, T., Pearson, D. M., Proud, M. B., Cheung, S. W., & Scott, D. A. (2009) · American Journal of Medical Genetics Part A · doi:10.1002/ajmg.a.32941 · Cited by 62
Colocalization of parvalbumin, calretinin and calbindin D-28k in human cortical and subcortical visual structures
Leuba, G., & Saini, K. (1997) · Journal of Chemical Neuroanatomy · doi:10.1016/s0891-0618(97)00022-7 · Cited by 55
No reduction of spindle neuron number in frontoinsular cortex in autism
Kennedy, D. P., Semendeferi, K., & Courchesne, E. (2007) · Brain and Cognition · doi:10.1016/j.bandc.2007.01.007 · Cited by 55
Chandelier cell axons are immunoreactive for GAT-1 in the human neocortex
DeFelipe, J., & González-Albo, M. D. C. (1998) · Neuroreport · doi:10.1097/00001756-199802160-00020 · Cited by 54
Developmental abnormalities of cortical interneurons precede symptoms onset in a mouse model of Rett syndrome
Tomassy, G. S., Morello, N., Calcagno, E., & Giustetto, M. (2014) · Journal of Neurochemistry · doi:10.1111/jnc.12803 · Cited by 49
Family‐based studies indicate association of Engrailed 2 gene with autism in an Indian population
Sen, B., Singh, A. S., Sinha, S., Chatterjee, A., Ahmed, S. S. S. J., Ghosh, S., & Rajamma, U. (2009) · Genes Brain & Behavior · doi:10.1111/j.1601-183x.2009.00556.x · Cited by 48
Evidence for association between Disrupted-in-schizophrenia 1 (DISC1) gene polymorphisms and autism in Chinese Han population: a family-based association study
Zheng, F., Wang, L.-F., Jia, M.-X., Yue, W., Ruan, Y., Lu, T.-L., Liu, J., Li, J., & Zhang, D. (2011) · Behavioral and Brain Functions · doi:10.1186/1744-9081-7-14 · Cited by 45
Alterations of GABAergic and dopaminergic systems in mutant mice with disruption of exons 2 and 3 of the Disc1 gene
NAKAI, T., Nagai, T., Wang, R., Yamada, S., Kuroda, K., Kaibuchi, K., & Yamada, K. (2014) · Neurochemistry International · doi:10.1016/j.neuint.2014.06.009 · Cited by 41
DISC1 duplication in two brothers with autism and mild mental retardation
Crepel, A., Breckpot, J., Fryns, J., la Marche, W. D., Steyaert, J. G., Devriendt, K., & Peeters, H. (2009) · Clinical Genetics · doi:10.1111/j.1399-0004.2009.01318.x · Cited by 33
Gamma‐band activity in the human superior temporal sulcus during mentalizing from nonverbal social cues
Cohen, M. X., David, N., Vogeley, K., & Elger, C. E. (2009) · Psychophysiology · doi:10.1111/j.1469-8986.2008.00724.x · Cited by 31
RELN-expressing neuron density in layer I of the superior temporal lobe is similar in human brains with autism and in age-matched controls
Camacho, J., Ejaz, E., Ariza, J., Noctor, S. C., & Martínez-Cerdeño, V. (2014) · Neuroscience Letters · doi:10.1016/j.neulet.2014.07.031 · Cited by 25
Self-citation
Calcium‐binding proteins in focal cortical dysplasia
Kuchukhidze, G., Wieselthaler, A., Drexel, M., Unterberger, I., Luef, G., Ortler, M., Becker, A. J., Trinka, E., & Sperk, G. (2015) · Epilepsia · doi:10.1111/epi.13053 · Cited by 22
Children with Autism Spectrum Disorder and Epilepsy
Francis, A., Msall, M. E., Obringer, E., & Kelley, K. R. (2013) · Pediatric Annals · doi:10.3928/00904481-20131122-10 · Cited by 22
Neuropathology of the posteroinferior occipitotemporal gyrus in children with autism
Uppal, N., Gianatiempo, I., Wicinski, B. A., Schmeidler, J., Heinsen, H., Schmitz, C., Buxbaum, J. D., & Hof, P. R. (2014) · Molecular Autism · doi:10.1186/2040-2392-5-17 · Cited by 18
Preliminary findings suggest the number and volume of supragranular and infragranular pyramidal neurons are similar in the anterior superior temporal area of control subjects and subjects with autism
Kim, E., Camacho, J., Combs, Z., Ariza, J., Lechpammer, M., Noctor, S. C., & Martínez-Cerdeño, V. (2015) · Neuroscience Letters · doi:10.1016/j.neulet.2015.01.021 · Cited by 17
Self-citation
Correction: G. Bradley Schaefer. Clinical Genetic Aspects of ASD Spectrum Disorders. Int. J. Mol. Sci. 2016, 17, 180
Schaefer, G. B. (2016) · International Journal of Molecular Sciences · doi:10.3390/ijms17091572 · Cited by 16
Association study of DISC1 in Korean population with autism spectrum disorders
Lim, S. M., Kim, H., Nam, M., Chung, J., & Park, Y. H. (2009) · Psychiatric Genetics · doi:10.1097/ypg.0b013e32832a9bd1 · Cited by 12
Untitled work
Defelipe (1999) · doi:10.1002/(sici)1096-9861(19990927)412:3

Research works printed but not linked: 1

von Economo C . 1929. The cytoarchitectonics of the human cerebral cortex. London: Humphrey Milford - Oxford University.

Sorted by citations

Autism spectrum disorder: neuropathology and animal models
Varghese, M., Keshav, N., Jacot-Descombes, S., Warda, T., Wicinski, B., Dickstein, D. L., Harony-Nicolas, H., De Rubeis, S., Drapeau, E., Buxbaum, J. D., et al. (2017) · Acta Neuropathologica · doi:10.1007/s00401-017-1736-4 · Cited by 536
Development of prefrontal cortex
Kolk, S. M., & Rakic, P. (2022) · Neuropsychopharmacology · doi:10.1038/s41386-021-01137-9 · Cited by 378
Oxidative stress-driven parvalbumin interneuron impairment as a common mechanism in models of schizophrenia
Steullet, P., Cabungcal, J.-H., Coyle, J., Didriksen, M., Gill, K., Grace, A. A., Hensch, T. K., LaMantia, A.-S., Lindemann, L., Maynard, T. M., et al. (2017) · Molecular Psychiatry · doi:10.1038/mp.2017.47 · Cited by 360
Medial prefrontal cortex in neurological diseases
Xu, P., Chen, A., Li, Y., Xing, X., & Lü, H. (2019) · Physiological Genomics · doi:10.1152/physiolgenomics.00006.2019 · Cited by 360
Modulation of prefrontal cortex excitation/inhibition balance rescues social behavior in CNTNAP2 -deficient mice
Selimbeyoglu, A., Kim, C. K., Inoue, M., Lee, S. Y., Hong, A. S. O., Kauvar, I., Ramakrishnan, C., Fenno, L. E., Davidson, T. J., Wright, M., et al. (2017) · Science Translational Medicine · doi:10.1126/scitranslmed.aah6733 · Cited by 326

See all 322

Authors: Hashemi, E., Ariza, J., Rogers, H., Noctor, S. C., & Martínez-Cerdeño, V.
Affiliations: Shriners Hospitals for Children - Northern California (US)
University of California Davis Medical Center (US)
ORCID: Hashemi, Ezzat
Noctor, Stephen C.
Venue: Cerebral Cortex
Publisher: Oxford University Press (OUP)
Published: 2016-02-27
Volume: 27
Issue: 2
Pages: bhw021
ISSN: 1047-3211 (ISSN-L)
1460-2199
DOI: 10.1093/cercor/bhw021
PMC: PMC6074948
OpenAlex: W2294392975
Cited by: 322
References: 113
Citations by year: 2026: 17 · 2025: 20 · 2024: 32 · 2023: 30 · 2022: 26 · 2021: 49 · 2020: 45 · 2019: 34 · 2018: 30 · 2017: 32 · 2016: 7
FWCI: 21.85
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Cerebral Cortex (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
eScholarship (California Digital Library) (submittedVersion)
Funders: National Institute for Mental Health (MH094681 and MH101188)
MIND Institute (U54 HD079125)
Shriners Hospitals, and the Pathology Department at UCD
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Autism Spectrum Disorder Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords: autism spectrum disorder, parvalbumin interneurons, GABAergic interneurons, medial prefrontal cortex, excitation-inhibition balance, interneuron subtypes, calbindin, calretinin, fast-spiking interneurons, gamma oscillations, postmortem brain
MeSH terms: Adolescent, Adult, Autistic Disorder, Cell Count, Child, Female, Humans, Interneurons, Male, Middle Aged, Parvalbumins, Calbindins, Calbindin 2

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

The Number of Parvalbumin-Expressing Interneurons Is Decreased in the Medial Prefrontal Cortex in Autism

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Self-check

Citations

Cites

Cited by

Related

Metadata

Record

About these checks