Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Altered excitatory and inhibitory ionotropic receptor subunit expression in the cortical visuospatial working memory network in schizophrenia

Neuropsychopharmacology (2024)Cite this article

Subjects

Abstract

Dysfunction of the cortical dorsal visual stream and visuospatial working memory (vsWM) network in individuals with schizophrenia (SZ) likely reflects alterations in both excitatory and inhibitory neurotransmission within nodes responsible for information transfer across the network, including primary visual (V1), visual association (V2), posterior parietal (PPC), and dorsolateral prefrontal (DLPFC) cortices. However, the expression patterns of ionotropic glutamatergic and GABAergic receptor subunits across these regions, and alterations of these patterns in SZ, have not been investigated. We quantified transcript levels of key subunits for excitatory N-methyl-D-aspartate receptors (NMDARs), excitatory alpha-amino-3-hydroxy-5-methyl-4-isoxazole propionic acid receptors (AMPARs), and inhibitory GABAA receptors (GABAARs) in postmortem total gray matter from V1, V2, PPC, and DLPFC of unaffected comparison (UC) and matched SZ subjects. In UC subjects, levels of most AMPAR and NMDAR mRNAs exhibited opposite rostral-to-caudal gradients, with AMPAR GRIA1 and GRIA2 mRNA levels highest in DLPFC and NMDAR GRIN1 and GRIN2A mRNA levels highest in V1. GABRA5 and GABRA1 mRNA levels were highest in DLPFC and V1, respectively. In SZ, most transcript levels were lower relative to UC subjects, with these differences largest in V1, intermediate in V2 and PPC, and smallest in DLPFC. In UC subjects, these distinct patterns of receptor transcript levels across the cortical vsWM network suggest that the balance between excitation and inhibition is achieved in a region-specific manner. In SZ subjects, the large deficits in excitatory and inhibitory receptor transcript levels in caudal sensory regions suggest that abnormalities early in the vsWM pathway might contribute to altered information processing in rostral higher-order regions.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Glutamate and GABAAR subunit transcript levels in the cortical vsWM network of unaffected comparison individuals.
Fig. 2: Box and whisker plots of glutamate receptor subunit transcript levels in the cortical vsWM network of unaffected comparison individuals (UC; open bars) and individuals with schizophrenia (SZ; filled bars).
Fig. 3: Box and whisker plots of GABAAR subunit transcript levels in the cortical vsWM network of unaffected comparison individuals (UC; open bars) and individuals with schizophrenia (SZ; filled bars).
Fig. 4: Glutamate receptor and GABAAR subunit transcript ratio levels in the cortical vsWM network of unaffected comparison individuals (UC; open bars) and individuals with schizophrenia (SZ; filled bars).

Similar content being viewed by others

Data availability

Individual subject data are shown in the figures, and both deidentified subject data and R code for the analysis will be provided upon request.

References

  1. Baddeley A. Working memory. Science. 1992;255:556–9.

    Article  CAS  PubMed  Google Scholar 

  2. Eriksson J, Vogel EK, Lansner A, Bergström F, Nyberg L. Neurocognitive architecture of working memory. Neuron. 2015;88:33–46.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Christophel TB, Klink PC, Spitzer B, Roelfsema PR, Haynes JD. The distributed nature of working memory. Trends Cogn Sci. 2017;21:111–24.

    Article  PubMed  Google Scholar 

  4. Henseler I, Falkai P, Gruber O. A systematic fMRI investigation of the brain systems subserving different working memory components in schizophrenia. Eur J Neurosci. 2009;30:693–702.

    Article  CAS  PubMed  Google Scholar 

  5. Henseler I, Falkai P, Gruber O. Disturbed functional connectivity within brain networks subserving domain-specific subcomponents of working memory in schizophrenia: relation to performance and clinical symptoms. J Psychiatr Res. 2010;44:364–72.

    Article  PubMed  Google Scholar 

  6. Meyer-Lindenberg A, Poline JB, Kohn PD, Holt JL, Egan MF, Weinberger DR, et al. Evidence for abnormal cortical functional connectivity during working memory in schizophrenia. Am J Psychiatry. 2001;158:1809–17.

    Article  CAS  PubMed  Google Scholar 

  7. Schlösser R, Gesierich T, Kaufmann B, Vucurevic G, Hunsche S, Gawehn J, et al. Altered effective connectivity during working memory performance in schizophrenia: a study with fMRI and structural equation modeling. Neuroimage. 2003;19:751–63.

    Article  PubMed  Google Scholar 

  8. Müller NG, Knight RT. The functional neuroanatomy of working memory: contributions of human brain lesion studies. Neuroscience. 2006;139:51–8.

    Article  PubMed  Google Scholar 

  9. Repovš G, Barch DM. Working memory related brain network connectivity in individuals with schizophrenia and their siblings. Front Hum Neurosci. 2012;6:137.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Constantinidis C, Williams GV, Goldman-Rakic PS. A role for inhibition in shaping the temporal flow of information in prefrontal cortex. Nat Neurosci. 2002;5:175–80.

    Article  CAS  PubMed  Google Scholar 

  11. Fish KN, Rocco BR, DeDionisio AM, Dienel SJ, Sweet RA, Lewis DA. Altered parvalbumin basket cell terminals in the cortical visuospatial working memory network in schizophrenia. Biol Psychiatry. 2021;90:47–57.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Hoftman GD, Dienel SJ, Bazmi HH, Zhang Y, Chen K, Lewis DA. Altered gradients of glutamate and gamma-aminobutyric acid transcripts in the cortical visuospatial working memory network in schizophrenia. Biol Psychiatry. 2018;83:670–79.

    Article  CAS  PubMed  Google Scholar 

  13. Tsubomoto M, Kawabata R, Zhu X, Minabe Y, Chen K, Lewis DA, et al. Expression of transcripts selective for GABA neuron subpopulations across the cortical visuospatial working memory network in the healthy state and schizophrenia. Cereb Cortex. 2019;29:3540–50.

    Article  PubMed  Google Scholar 

  14. Akbarian S, Liu C, Knowles JA, Vaccarino FM, Farnham PJ, Crawford GE, et al. The PsychENCODE project. Nat Neurosci. 2015;18:1707–12.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Hawrylycz MJ, Lein ES, Guillozet-Bongaarts AL, Shen EH, Ng L, Miller JA, et al. An anatomically comprehensive atlas of the adult human brain transcriptome. Nature. 2012;489:391–99.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Kang HJ, Kawasawa YI, Cheng F, Zhu Y, Xu X, Li M, et al. Spatio-temporal transcriptome of the human brain. Nature. 2011;478:483–9.

  17. Sieghart W. Structure and pharmacology of gamma-aminobutyric acidA receptor subtypes. Pharmacol Rev. 1995;47:181–234.

    CAS  PubMed  Google Scholar 

  18. Isaac JT, Ashby MC, McBain CJ. The role of the GluR2 subunit in AMPA receptor function and synaptic plasticity. Neuron. 2007;54:859–71.

    Article  CAS  PubMed  Google Scholar 

  19. Traynelis SF, Wollmuth LP, McBain CJ, Menniti FS, Vance KM, Ogden KK, et al. Glutamate receptor ion channels: structure, regulation, and function. Pharmacol Rev. 2010;62:405–96.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Paoletti P, Bellone C, Zhou Q. NMDA receptor subunit diversity: impact on receptor properties, synaptic plasticity and disease. Nat Rev Neurosci. 2013;14:383–400.

    Article  CAS  PubMed  Google Scholar 

  21. Lu W, Shi Y, Jackson AC, Bjorgan K, During MJ, Sprengel R, et al. Subunit composition of synaptic AMPA receptors revealed by a single-cell genetic approach. Neuron. 2009;62:254–68.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Mayer ML, Armstrong N. Structure and function of glutamate receptor ion channels. Annu Rev Physiol. 2004;66:161–81.

    Article  CAS  PubMed  Google Scholar 

  23. Monyer H, Sprengel R, Schoepfer R, Herb A, Higuchi M, Lomeli H, et al. Heteromeric NMDA receptors: molecular and functional distinction of subtypes. Science. 1992;256:1217–21.

    Article  CAS  PubMed  Google Scholar 

  24. Monyer H, Burnashev N, Laurie DJ, Sakmann B, Seeburg PH. Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron. 1994;12:529–40.

    Article  CAS  PubMed  Google Scholar 

  25. Ali AB, Thomson AM. Synaptic alpha 5 subunit-containing GABAA receptors mediate IPSPs elicited by dendrite-preferring cells in rat neocortex. Cereb Cortex. 2008;18:1260–71.

    Article  PubMed  Google Scholar 

  26. Silberberg G, Markram H. Disynaptic inhibition between neocortical pyramidal cells mediated by Martinotti cells. Neuron. 2007;53:735–46.

    Article  CAS  PubMed  Google Scholar 

  27. Klausberger T, Roberts JD, Somogyi P. Cell type- and input-specific differences in the number and subtypes of synaptic GABA(A) receptors in the hippocampus. J Neurosci. 2002;22:2513–21.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Fritschy JM, Mohler H. GABAA-receptor heterogeneity in the adult rat brain: differential regional and cellular distribution of seven major subunits. J Comp Neurol. 1995;359:154–94.

    Article  CAS  PubMed  Google Scholar 

  29. Angelotti TP, Macdonald RL. Assembly of GABAA receptor subunits: alpha 1 beta 1 and alpha 1 beta 1 gamma 2S subunits produce unique ion channels with dissimilar single-channel properties. J Neurosci. 1993;13:1429–40.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Alldred MJ, Mulder-Rosi J, Lingenfelter SE, Chen G, Lüscher B. Distinct gamma2 subunit domains mediate clustering and synaptic function of postsynaptic GABAA receptors and gephyrin. J Neurosci. 2005;25:594–603.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Roussy M, Luna R, Duong L, Corrigan B, Gulli RA, Nogueira R, et al. Ketamine disrupts naturalistic coding of working memory in primate lateral prefrontal cortex networks. Mol Psychiatry. 2021;26:6688–703.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Ranganathan M, DeMartinis N, Huguenel B, Gaudreault F, Bednar MM, Shaffer CL, et al. Attenuation of ketamine-induced impairment in verbal learning and memory in healthy volunteers by the AMPA receptor potentiator PF-04958242. Mol Psychiatry. 2017;22:1633–40.

    Article  CAS  PubMed  Google Scholar 

  33. Rao SG, Williams GV, Goldman-Rakic PS. Destruction and creation of spatial tuning by disinhibition: GABA(A) blockade of prefrontal cortical neurons engaged by working memory. J Neurosci. 2000;20:485–94.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Glausier JR, Kelly MA, Salem S, Chen K, Lewis DA. Proxy measures of premortem cognitive aptitude in postmortem subjects with schizophrenia. Psychol Med. 2020;50:507–14.

    Article  PubMed  Google Scholar 

  35. Chung DW, Chung Y, Bazmi HH, Lewis DA. Altered ErbB4 splicing and cortical parvalbumin interneuron dysfunction in schizophrenia and mood disorders. Neuropsychopharmacology. 2018;43:2478–86.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Chomczynski P. A reagent for the single-step simultaneous isolation of RNA, DNA and proteins from cell and tissue samples. Biotechniques. 1993;15:532–4.

    CAS  PubMed  Google Scholar 

  37. Kimoto S, Hashimoto T, Berry KJ, Tsubomoto M, Yamaguchi Y, Enwright JF, et al. Expression of actin- and oxidative phosphorylation-related transcripts across the cortical visuospatial working memory network in unaffected comparison and schizophrenia subjects. Neuropsychopharmacology. 2022;47:2061–70.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Kuznetsova A, Brockhoff PB, Rune HB. {lmerTest} Package: tests in linear mixed effects models. J Stat Softw. 2017;82:1–26.

    Article  Google Scholar 

  39. Hotelling H. The generalization of student’s ratio. Ann Math Stat. 1931;2:360–78.

    Article  Google Scholar 

  40. Enwright Iii JF, Arion D, MacDonald WA, Elbakri R, Pan Y, Vyas G, et al. Differential gene expression in layer 3 pyramidal neurons across 3 regions of the human cortical visual spatial working memory network. Cereb Cortex. 2022;32:5216–29.

    Article  PubMed  PubMed Central  Google Scholar 

  41. Enwright Iii JF, Huo Z, Arion D, Corradi JP, Tseng G, Lewis DA. Transcriptome alterations of prefrontal cortical parvalbumin neurons in schizophrenia. Mol Psychiatry. 2018;23:1606–13.

  42. Enwright JF, Sanapala S, Foglio A, Berry R, Fish KN, Lewis DA. Reduced labeling of parvalbumin neurons and perineuronal nets in the dorsolateral prefrontal cortex of subjects with schizophrenia. Neuropsychopharmacology. 2016;41:2206–14.

    Article  PubMed  PubMed Central  Google Scholar 

  43. Di Maio V, Ventriglia F, Santillo S. AMPA/NMDA cooperativity and integration during a single synaptic event. J Comput Neurosci. 2016;41:127–42.

    Article  PubMed  Google Scholar 

  44. Sheng M, Cummings J, Roldan LA, Jan YN, Jan LY. Changing subunit composition of heteromeric NMDA receptors during development of rat cortex. Nature. 1994;368:144–47.

    Article  CAS  PubMed  Google Scholar 

  45. Torres-Gomez S, Blonde JD, Mendoza-Halliday D, Kuebler E, Everest M, Wang XJ, et al. Changes in the proportion of inhibitory interneuron types from sensory to executive areas of the primate neocortex: implications for the origins of working memory representations. Cereb Cortex. 2020;30:4544–62.

    Article  PubMed  PubMed Central  Google Scholar 

  46. Dienel SJ, Ciesielski AJ, Bazmi HH, Profozich EA, Fish KN, Lewis DA. Distinct laminar and cellular patterns of GABA neuron transcript expression in monkey prefrontal and visual cortices. Cereb Cortex. 2021;31:2345–63.

    Article  PubMed  Google Scholar 

  47. Chen A, Sun Y, Lei Y, Li C, Liao S, Meng J, et al. Single-cell spatial transcriptome reveals cell-type organization in the macaque cortex. Cell. 2023;186:3726–43.e24.

    Article  CAS  PubMed  Google Scholar 

  48. Zilles K, Palomero-Gallagher N. Multiple transmitter receptors in regions and layers of the human cerebral cortex. Front Neuroanat. 2017;11:78.

    Article  PubMed  PubMed Central  Google Scholar 

  49. Horn ME, Nicoll RA. Somatostatin and parvalbumin inhibitory synapses onto hippocampal pyramidal neurons are regulated by distinct mechanisms. Proc Natl Acad Sci USA. 2018;115:589–94.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. de Lima AD, Morrison JH. Ultrastructural analysis of somatostatin-immunoreactive neurons and synapses in the temporal and occipital cortex of the macaque monkey. J Comp Neurol. 1989;283:212–27.

    Article  PubMed  Google Scholar 

  51. Melchitzky DS, Lewis DA. Dendritic-targeting GABA neurons in monkey prefrontal cortex: comparison of somatostatin- and calretinin-immunoreactive axon terminals. Synapse. 2008;62:456–65.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Xu H, Jeong H-Y, Tremblay R, Rudy B. Neocortical somatostatin-expressing GABAergic interneurons disinhibit the thalamorecipient layer 4. Neuron. 2013;77:155–67.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Williams SM, Goldman-Rakic PS, Leranth C. The synaptology of parvalbumin-immunoreactive neurons in the primate prefrontal cortex. J Comp Neurol. 1992;320:353–69.

    Article  CAS  PubMed  Google Scholar 

  54. Freund TF, Katona I. Perisomatic inhibition. Neuron. 2007;56:33–42.

    Article  CAS  PubMed  Google Scholar 

  55. Hashimoto T, Arion D, Unger T, Maldonado-Aviles JG, Morris HM, Volk DW, et al. Alterations in GABA-related transcriptome in the dorsolateral prefrontal cortex of subjects with schizophrenia. Mol Psychiatry. 2008;13:147–61.

    Article  CAS  PubMed  Google Scholar 

  56. Beneyto M, Abbott A, Hashimoto T, Lewis DA. Lamina-specific alterations in cortical GABAA receptor subunit expression in schizophrenia. Cereb Cortex. 2011;21:999–1011.

    Article  PubMed  Google Scholar 

  57. Duncan CE, Webster MJ, Rothmond DA, Bahn S, Elashoff M, Shannon Weickert C, et al. receptor alpha-subunit expression in normal postnatal human development and schizophrenia. J Psychiatr Res. 2010;44:673–81.

    Article  PubMed  Google Scholar 

  58. Beneyto M, Meador-Woodruff JH. Lamina-specific abnormalities of AMPA receptor trafficking and signaling molecule transcripts in the prefrontal cortex in schizophrenia. Synapse. 2006;60:585–98.

    Article  CAS  PubMed  Google Scholar 

  59. Dracheva S, McGurk SR, Haroutunian V. mRNA expression of AMPA receptors and AMPA receptor binding proteins in the cerebral cortex of elderly schizophrenics. J Neurosci Res. 2005;79:868–78.

    Article  CAS  PubMed  Google Scholar 

  60. Weickert CS, Fung SJ, Catts VS, Schofield PR, Allen KM, Moore LT, et al. Molecular evidence of N-methyl-D-aspartate receptor hypofunction in schizophrenia. Mol Psychiatry. 2013;18:1185–92.

    Article  CAS  PubMed  Google Scholar 

  61. Akbarian S, Sucher NJ, Bradley D, Tafazzoli A, Trinh D, Hetrick WP, et al. Selective alterations in gene expression for NMDA receptor subunits in prefrontal cortex of schizophrenics. J Neurosci. 1996;16:19–30.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Beneyto M, Meador-Woodruff JH. Lamina-specific abnormalities of NMDA receptor-associated postsynaptic protein transcripts in the prefrontal cortex in schizophrenia and bipolar disorder. Neuropsychopharmacology. 2008;33:2175–86.

    Article  CAS  PubMed  Google Scholar 

  63. Sokolov BP. Expression of NMDAR1, GluR1, GluR7, and KA1 glutamate receptor mRNAs is decreased in frontal cortex of “neuroleptic-free” schizophrenics: evidence on reversible up-regulation by typical neuroleptics. J Neurochem. 1998;71:2454–64.

    Article  CAS  PubMed  Google Scholar 

  64. Hashimoto T, Bazmi HH, Mirnics K, Wu Q, Sampson AR, Lewis DA. Conserved regional patterns of GABA-related transcript expression in the neocortex of subjects with schizophrenia. Am J Psychiatry. 2008;165:479–89.

    Article  PubMed  PubMed Central  Google Scholar 

  65. Glantz LA, Lewis DA. Decreased dendritic spine density on prefrontal cortical pyramidal neurons in schizophrenia. Arch Gen Psychiatry. 2000;57:65–73.

    Article  CAS  PubMed  Google Scholar 

  66. Glausier JR, Enwright JF 3rd, Lewis DA. Diagnosis- and cell type-specific mitochondrial functional pathway signatures in schizophrenia and bipolar disorder. Am J Psychiatry. 2020;177:1140–50.

    Article  PubMed  PubMed Central  Google Scholar 

  67. Schoonover KE, Dienel SJ, Lewis DA. Prefrontal cortical alterations of glutamate and GABA neurotransmission in schizophrenia: Insights for rational biomarker development. Biomark Neuropsychiatry. 2020;3:100015.

    Article  PubMed  PubMed Central  Google Scholar 

  68. Schoonover KE, Miller NE, Fish KN, Lewis DA. Scaling of smaller pyramidal neuron size and lower energy production in schizophrenia. Neurobiol Dis. 2024;191:106394.

    Article  PubMed  PubMed Central  Google Scholar 

  69. Qian N, Lipkin RM, Kaszowska A, Silipo G, Dias EC, Butler PD, et al. Computational modeling of excitatory/inhibitory balance impairments in schizophrenia. Schizophr Res. 2022;249:47–55.

    Article  CAS  PubMed  Google Scholar 

  70. Hoffmann H, Gremme T, Hatt H, Gottmann K. Synaptic activity-dependent developmental regulation of NMDA receptor subunit expression in cultured neocortical neurons. J Neurochem. 2000;75:1590–9.

    Article  CAS  PubMed  Google Scholar 

  71. Glausier JR, Lewis DA. Dendritic spine pathology in schizophrenia. Neuroscience. 2013;251:90–107.

    Article  CAS  PubMed  Google Scholar 

  72. Singh T, Poterba T, Curtis D, Akil H, Al Eissa M, Barchas JD, et al. Rare coding variants in ten genes confer substantial risk for schizophrenia. Nature. 2022;604:509–16.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Javitt DC. When doors of perception close: bottom-up models of disrupted cognition in schizophrenia. Annu Rev Clin Psychol. 2009;5:249–75.

    Article  PubMed  PubMed Central  Google Scholar 

  74. Butler PD, Zemon V, Schechter I, Saperstein AM, Hoptman MJ, Lim KO, et al. Early-stage visual processing and cortical amplification deficits in schizophrenia. Arch Gen Psychiatry. 2005;62:495–504.

    Article  PubMed  PubMed Central  Google Scholar 

  75. Dias EC, Butler PD, Hoptman MJ, Javitt DC. Early sensory contributions to contextual encoding deficits in schizophrenia. Arch Gen Psychiatry. 2011;68:654–64.

    Article  PubMed  PubMed Central  Google Scholar 

  76. Dias EC, Bickel S, Epstein ML, Sehatpour P, Javitt DC. Abnormal task modulation of oscillatory neural activity in schizophrenia. Front Psychol. 2013;4:540.

    Article  PubMed  PubMed Central  Google Scholar 

  77. Dias EC, Van Voorhis AC, Braga F, Todd J, Lopez-Calderon J, Martinez A, et al. Impaired fixation-related theta modulation predicts reduced visual span and guided search deficits in schizophrenia. Cereb Cortex. 2020;30:2823–33.

    Article  PubMed  PubMed Central  Google Scholar 

  78. Rajkai C, Lakatos P, Chen CM, Pincze Z, Karmos G, Schroeder CE. Transient cortical excitation at the onset of visual fixation. Cereb Cortex. 2008;18:200–9.

    Article  PubMed  Google Scholar 

  79. Arnsten AF. Prefrontal cortical network connections: key site of vulnerability in stress and schizophrenia. Int J Dev Neurosci. 2011;29:215–23.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

Brain tissue for this study was provided by the University of Pittsburgh Brain Tissue Donation Program. We thank Kelly Rogers for tissue sample preparation. Most importantly, we thank all the family members who donated tissue.

Funding

This work was supported by the National Institute of Mental Health (grant numbers NIMH043784 to DAL, NIMH122943 to KES).

Author information

Authors and Affiliations

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

    Kirsten E. Schoonover, Samuel J. Dienel, H. Holly Bazmi, John F. Enwright III & David A. Lewis

  2. Department of Psychiatry and Behavioral Neurobiology, School of Medicine, University of Alabama at Birmingham, Birmingham, AL, USA

    Kirsten E. Schoonover

  3. Department of Neuroscience, Dietrich School of Arts and Sciences, University of Pittsburgh, Pittsburgh, PA, USA

    Samuel J. Dienel & David A. Lewis

  4. Center for the Neural Basis of Cognition, Carnegie Mellon University, Pittsburgh, PA, USA

    Samuel J. Dienel & David A. Lewis

Authors
  1. Kirsten E. Schoonover
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Samuel J. Dienel
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. H. Holly Bazmi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. John F. Enwright III
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. David A. Lewis
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Authors Schoonover, Dienel, Bazmi, Enwright, and Lewis were responsible for experimental design and data analysis. Author Bazmi was responsible for qPCR primer design and experimental execution. All authors were involved in manuscript preparation and editing.

Corresponding author

Correspondence to David A. Lewis.

Ethics declarations

Competing interests

DL currently receives research funding from Merck for work unrelated to these studies. All other authors report no competing interests.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Schoonover, K.E., Dienel, S.J., Holly Bazmi, H. et al. Altered excitatory and inhibitory ionotropic receptor subunit expression in the cortical visuospatial working memory network in schizophrenia. Neuropsychopharmacol. (2024). https://doi.org/10.1038/s41386-024-01854-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1038/s41386-024-01854-x

Search

Advanced search

Quick links