OpenLB
Open Library of Bioscience
Advanced Search
Cerebral cortex (New York, N.Y. : 1991)
03 05, 2021;31 (4): 2026-2037.

Postnatal Development of Glutamate and GABA Transcript Expression in Monkey Visual, Parietal, and Prefrontal Cortices.

Gil D Hoftman, H Holly Bazmi, Andrew J Ciesielski, Liban A Dinka, Kehui Chen, David A Lewis
Author Information
  1. Gil D Hoftman: Department of Psychiatry, University of California, Los Angeles, CA 90095, USA.
  2. H Holly Bazmi: Department of Psychiatry, School of Medicine, University of Pittsburgh, Pittsburgh, PA 15213, USA.
  3. Andrew J Ciesielski: Department of Psychiatry, School of Medicine, University of Pittsburgh, Pittsburgh, PA 15213, USA.
  4. Liban A Dinka: Department of Psychiatry, School of Medicine, University of Pittsburgh, Pittsburgh, PA 15213, USA.
  5. Kehui Chen: Department of Statistics, School of Arts and Sciences, University of Pittsburgh, Pittsburgh, PA 15213, USA.
  6. David A Lewis: Department of Psychiatry, School of Medicine, University of Pittsburgh, Pittsburgh, PA 15213, USA.
PMID: 33279960 DOI: 10.1093/cercor/bhaa342

Abstract

Visuospatial working memory (vsWM) requires information transfer among multiple cortical regions, from primary visual (V1) to prefrontal (PFC) cortices. This information is conveyed via layer 3 glutamatergic neurons whose activity is regulated by gamma-aminobutyric acid (GABA)ergic interneurons. In layer 3 of adult human neocortex, molecular markers of glutamate neurotransmission were lowest in V1 and highest in PFC, whereas GABA markers had the reverse pattern. Here, we asked if these opposite V1-visual association cortex (V2)-posterior parietal cortex (PPC)-PFC gradients across the vsWM network are present in layer 3 of monkey neocortex, when they are established during postnatal development, and if they are specific to this layer. We quantified transcript levels of glutamate and GABA markers in layers 3 and 6 of four vsWM cortical regions in a postnatal developmental series of 30 macaque monkeys. In adult monkeys, glutamate transcript levels in layer 3 increased across V1-V2-PPC-PFC regions, whereas GABA transcripts showed the opposite V1-V2-PPC-PFC gradient. Glutamate transcripts established adult-like expression patterns earlier during postnatal development than GABA transcripts. These V1-V2-PPC-PFC gradients and developmental patterns were less evident in layer 6. These findings demonstrate that expression of glutamate and GABA transcripts differs across cortical regions and layers during postnatal development, revealing potential molecular substrates for vsWM functional maturation.

Keywords

GABA cortical regions development glutamate working memory

References

  1. Proc Natl Acad Sci U S A. 2016 Jan 19;113(3):740-5 [PMID: 26729880]
  2. J Neurol Neurosurg Psychiatry. 1998 Oct;65(4):446-53 [PMID: 9771764]
  3. J Comp Neurol. 2000 Dec 4;428(1):79-111 [PMID: 11058226]
  4. Neuron. 1995 Mar;14(3):477-85 [PMID: 7695894]
  5. J Neurosci. 1987 May;7(5):1503-19 [PMID: 3033170]
  6. JAMA Psychiatry. 2018 Dec 1;75(12):1252-1260 [PMID: 30285056]
  7. Schizophr Bull. 2015 Jan;41(1):180-91 [PMID: 24361861]
  8. Nat Neurosci. 2014 Dec;17(12):1661-3 [PMID: 25383900]
  9. Science. 1986 Apr 11;232(4747):232-5 [PMID: 3952506]
  10. Nat Rev Neurosci. 2009 Oct;10(10):724-35 [PMID: 19763105]
  11. Cell. 2017 Oct 5;171(2):456-469.e22 [PMID: 28985566]
  12. Cereb Cortex. 1993 Mar-Apr;3(2):148-62 [PMID: 8490320]
  13. Front Neuroanat. 2014 Aug 12;8:78 [PMID: 25161611]
  14. Nature. 2011 Oct 26;478(7370):483-9 [PMID: 22031440]
  15. J Comp Neurol. 1997 Oct 20;387(2):167-78 [PMID: 9336221]
  16. Proc Natl Acad Sci U S A. 2017 Jan 24;114(4):E629-E637 [PMID: 28074037]
  17. Science. 1992 Jan 31;255(5044):556-9 [PMID: 1736359]
  18. Genome Res. 2012 Apr;22(4):611-22 [PMID: 22300767]
  19. Neurobiol Dis. 2017 Sep;105:132-141 [PMID: 28576707]
  20. Cereb Cortex. 2008 Apr;18(4):915-29 [PMID: 17652464]
  21. Cereb Cortex. 1991 Jan-Feb;1(1):1-47 [PMID: 1822724]
  22. J Neurosci. 1992 Nov;12(11):4545-64 [PMID: 1331364]
  23. Proc Natl Acad Sci U S A. 2011 Aug 9;108(32):13281-6 [PMID: 21788513]
  24. Neuroscientist. 2007 Apr;13(2):115-26 [PMID: 17404372]
  25. Science. 2018 Dec 14;362(6420): [PMID: 30545855]
  26. Cereb Cortex. 2011 Apr;21(4):845-52 [PMID: 20732898]
  27. J Neurosci. 2001 Sep 1;21(17):RC163 [PMID: 11511694]
  28. Trends Neurosci. 2001 Aug;24(8):455-63 [PMID: 11476885]
  29. Nature. 2010 Nov 11;468(7321):203-12 [PMID: 21068828]
  30. Am J Psychiatry. 2005 Jun;162(6):1200-2 [PMID: 15930070]
  31. Nat Neurosci. 2015 Oct;18(10):1376-85 [PMID: 26404712]
  32. CNS Spectr. 2005 Oct;10(10):808-19 [PMID: 16400244]
  33. Neuron. 2015 Oct 21;88(2):419-31 [PMID: 26439530]
  34. Proc Natl Acad Sci U S A. 2004 Feb 3;101(5):1368-73 [PMID: 14742867]
  35. Arch Gen Psychiatry. 2000 Jan;57(1):65-73 [PMID: 10632234]
  36. Trends Neurosci. 2005 Oct;28(10):512-7 [PMID: 16126285]
  37. J Comp Neurol. 1993 Dec 15;338(3):360-76 [PMID: 8113445]
  38. J Neurosci. 2019 Sep 11;39(37):7277-7290 [PMID: 31341029]
  39. J Comp Neurol. 1991 Mar 15;305(3):370-92 [PMID: 1709953]
  40. Dev Neurobiol. 2011 Jan 1;71(1):18-33 [PMID: 21154907]
  41. Arch Gen Psychiatry. 2000 Mar;57(3):237-45 [PMID: 10711910]
  42. Nat Commun. 2018 Aug 29;9(1):3499 [PMID: 30158572]
  43. J Neurosci. 1993 Jul;13(7):2801-20 [PMID: 8331373]
  44. Trends Cogn Sci. 2012 Jan;16(1):27-34 [PMID: 22169777]
  45. Proc Natl Acad Sci U S A. 1996 Nov 26;93(24):13473-80 [PMID: 8942959]
  46. Arch Gen Psychiatry. 1998 Mar;55(3):215-24 [PMID: 9510215]
  47. J Comp Neurol. 1998 Mar 16;392(3):402-12 [PMID: 9511926]
  48. Nature. 2012 Sep 20;489(7416):391-399 [PMID: 22996553]
  49. J Neurosci. 2013 May 8;33(19):8352-8 [PMID: 23658174]
  50. Arch Gen Psychiatry. 1995 Apr;52(4):258-66 [PMID: 7702443]
  51. Nat Neurosci. 2018 Aug;21(8):1117-1125 [PMID: 30050107]
  52. Neuroscience. 1995 Jul;67(1):7-22 [PMID: 7477911]
  53. Nat Commun. 2020 Jun 8;11(1):2889 [PMID: 32514083]
  54. J Comp Neurol. 1977 Nov 15;176(2):149-88 [PMID: 410850]
  55. Curr Opin Neurobiol. 2018 Apr;49:75-83 [PMID: 29414069]
  56. Nat Genet. 2013 Jun;45(6):580-5 [PMID: 23715323]
  57. Front Neuroanat. 2017 Mar 07;11:11 [PMID: 28326020]
  58. Eur J Neurosci. 1999 Dec;11(12):4197-203 [PMID: 10594645]
  59. Am J Psychiatry. 2010 Feb;167(2):160-9 [PMID: 20048021]
  60. Neuroscience. 2013 Oct 22;251:90-107 [PMID: 22546337]
  61. Science. 1974 Feb 1;183(4123):425-7 [PMID: 4203022]
  62. Cereb Cortex. 2003 Nov;13(11):1124-38 [PMID: 14576205]
  63. Nat Neurosci. 2003 Mar;6(3):309-15 [PMID: 12548289]
  64. Neuropsychopharmacology. 2003 Mar;28(3):599-609 [PMID: 12629543]
  65. J Comp Neurol. 1996 Dec 23;376(4):614-30 [PMID: 8978474]
  66. Annu Rev Neurosci. 2001;24:167-202 [PMID: 11283309]
  67. Cell Biosci. 2020 Mar 4;10:26 [PMID: 32158532]
  68. Brain Res Dev Brain Res. 1996 Oct 23;96(1-2):261-76 [PMID: 8922688]
  69. Trends Pharmacol Sci. 2006 Mar;27(3):141-8 [PMID: 16490260]
  70. Cereb Cortex. 2015 Aug;25(8):2295-305 [PMID: 24610118]
  71. Neuroscientist. 2007 Jun;13(3):257-67 [PMID: 17519368]
  72. Nat Rev Neurosci. 2008 Mar;9(3):206-21 [PMID: 18270515]
  73. Annu Rev Neurosci. 2002;25:409-32 [PMID: 12052915]
  74. Schizophr Res. 2020 Mar;217:86-94 [PMID: 31296415]
  75. J Comp Neurol. 1995 Aug 14;359(1):131-43 [PMID: 8557842]
  76. Biol Psychiatry. 2018 Apr 15;83(8):670-679 [PMID: 29357982]
  77. Front Neurosci. 2017 Mar 13;11:118 [PMID: 28348514]
  78. Science. 2000 Aug 11;289(5481):957-60 [PMID: 10938000]
  79. Nature. 2000 Sep 14;407(6801):189-94 [PMID: 11001057]
  80. Cereb Cortex. 2008 Mar;18(3):626-37 [PMID: 17591597]
  81. Cereb Cortex. 2019 Jul 22;29(8):3540-3550 [PMID: 30247542]
  82. J Comp Neurol. 1982 Jan 10;204(2):196-210 [PMID: 6276450]
  83. Cereb Cortex. 2010 Mar;20(3):534-48 [PMID: 19520764]
  84. Cereb Cortex. 2014 Jan;24(1):17-36 [PMID: 23010748]
  85. J Comp Neurol. 1999 Sep 27;412(3):515-26 [PMID: 10441237]
  86. J Neurosci. 2000 Sep 15;20(18):RC95 [PMID: 10974092]
  87. J Comp Neurol. 2007 Mar 10;501(2):290-301 [PMID: 17226750]
  88. J Comp Neurol. 1994 Mar 1;341(1):95-116 [PMID: 8006226]
  89. J Neurosci. 2015 Jan 7;35(1):112-27 [PMID: 25568107]
  90. JAMA Psychiatry. 2014 Dec 1;71(12):1323-31 [PMID: 25271938]
  91. Nat Rev Neurosci. 2008 Feb;9(2):110-22 [PMID: 18209730]
  92. Cereb Cortex. 1994 Jan-Feb;4(1):78-96 [PMID: 8180493]

Grants

  1. R01 MH051234/NIMH NIH HHS
  2. T32 NS048004/NINDS NIH HHS

MeSH Term

Age Factors
Animals
Excitatory Amino Acid Transporter 2
Female
GABAergic Neurons
Gene Expression
Glutamic Acid
Macaca mulatta
Parietal Lobe
Prefrontal Cortex
Receptors, GABA-A
Transcription, Genetic
Visual Cortex
gamma-Aminobutyric Acid

Chemicals

Excitatory Amino Acid Transporter 2
GABRG2 protein, human
Receptors, GABA-A
SLC1A2 protein, human
Glutamic Acid
gamma-Aminobutyric Acid
Journal Article Research Support, N.I.H., Extramural

Word Cloud

Created with Highcharts 10.0.0GABAlayerregions3glutamatevsWMcorticalpostnataldevelopmenttranscriptsmarkersacrossV1-V2-PPC-PFCworkingmemoryinformationV1PFCadultneocortexmolecularwhereasoppositecortexgradientsestablishedtranscriptlevelslayers6developmentalmonkeysGlutamateexpressionpatternsVisuospatialrequirestransferamongmultipleprimaryvisualprefrontalcorticesconveyedviaglutamatergicneuronswhoseactivityregulatedgamma-aminobutyricacidergicinterneuronshumanneurotransmissionlowesthighestreversepatternaskedV1-visualassociationV2-posteriorparietalPPC-PFCnetworkpresentmonkeyspecificquantifiedfourseries30macaqueincreasedshowedgradientadult-likeearlierlessevidentfindingsdemonstratediffersrevealingpotentialsubstratesfunctionalmaturationPostnatalDevelopmentTranscriptExpressionMonkeyVisualParietalPrefrontalCortices

Similar Articles

Cited By