Cited by 196Neurotransmitter Receptor Influence on BehaviorNeuroscience and Neuropharmacology ResearchNeural and Behavioral Psychology Studies

Norepinephrine versus dopamine and their interaction in modulating synaptic function in the prefrontal cortex

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Xing, Bo, Li, Yan-Chun, Gao, Wen-Jun·2016·Brain Research

Abstract

Among the neuromodulators that regulate prefrontal cortical circuit function, the catecholamine transmitters norepinephrine (NE) and dopamine (DA) stand out as powerful players in working memory and attention. Perturbation of either NE or DA signaling is implicated in the pathogenesis of several neuropsychiatric disorders, including attention deficit hyperactivity disorder (ADHD), post-traumatic stress disorder (PTSD), schizophrenia, and drug addiction. Although the precise mechanisms employed by NE and DA to cooperatively control prefrontal functions are not fully understood, emerging research indicates that both transmitters regulate electrical and biochemical aspects of neuronal function by modulating convergent ionic and synaptic signaling in the prefrontal cortex (PFC). This review summarizes previous studies that investigated the effects of both NE and DA on excitatory and inhibitory transmissions in the prefrontal cortical circuitry. Specifically, we focus on the functional interaction between NE and DA in prefrontal cortical local circuitry, synaptic integration, signaling pathways, and receptor properties. Although it is clear that both NE and DA innervate the PFC extensively and modulate synaptic function by activating distinctly different receptor subtypes and signaling pathways, it remains unclear how these two systems coordinate their actions to optimize PFC function for appropriate behavior. Throughout this review, we provide perspectives and highlight several critical topics for future studies. This article is part of a Special Issue entitled SI: Noradrenergic System.

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  1. Agster KL Evidence for a regional specificity in the density and distribution of noradrenergic varicosities in rat cortex. J Comp Neurol 2013 521 2195 207 23184811 PMC4529674
  2. Aoki C Perikaryal and synaptic localization of alpha 2A-adrenergic receptor-like immunoreactivity. Brain Res 1994 650 181 204 7953684
  3. Aoki C Cellular and subcellular sites for noradrenergic action in the monkey dorsolateral prefrontal cortex as revealed by the immunocytochemical localization of noradrenergic receptors and axons. Cereb Cortex 1998a 8 269 77 9617922
  4. Aoki C Venkatesan C Kurose H Noradrenergic modulation of the prefrontal cortex as revealed by electron microscopic immunocytochemistry. Adv Pharmacol 1998b 42 777 80 9328013
  5. Arnsten AF Goldman-Rakic PS Noise stress impairs prefrontal cortical cognitive function in monkeys: evidence for a hyperdopaminergic mechanism. Arch Gen Psychiatry 1998 55 362 8 9554432
  6. Arnsten AF Alpha-1 noradrenergic receptor stimulation impairs prefrontal cortical cognitive function. Biol Psychiatry 1999 45 26 31 9894572
  7. Arnsten AF Stress impairs prefrontal cortical function in rats and monkeys: role of dopamine D1 and norepinephrine alpha-1 receptor mechanisms. Prog Brain Res 2000 126 183 92 11105647
  8. Arnsten AF Adrenergic targets for the treatment of cognitive deficits in schizophrenia. Psychopharmacology (Berl) 2004 174 25 31 15205875
  9. Arnsten AF Pliszka SR Catecholamine influences on prefrontal cortical function: relevance to treatment of attention deficit/hyperactivity disorder and related disorders. Pharmacol Biochem Behav 2011 99 211 6 21295057 PMC3129015
  10. Arnsten AF Jin LE Molecular influences on working memory circuits in dorsolateral prefrontal cortex. Prog Mol Biol Transl Sci 2014 122 211 31 24484703
  11. Arnsten Amy F.T. Wang Min J. Paspalas Constantinos D. Neuromodulation of thought: flexibilities and vulnerabilities in prefrontal cortical network synapses. Neuron 2012b 76 223 239 23040817 PMC3488343
  12. Arnsten AFT The effects of stress exposure on prefrontal cortex: Translating basic research into successful treatments for post-traumatic stress disorder. Neurobiology of Stress 2015b 1 89 99 25436222 PMC4244027
  13. Aston-Jones G Cohen JD An integrative theory of locus coeruleus-norepinephrine function: adaptive gain and optimal performance. Annu Rev Neurosci 2005 28 403 50 16022602
  14. Bacci A Huguenard JR Prince DA Modulation of neocortical interneurons: extrinsic influences and exercises in self-control. Trends Neurosci 2005 28 602 10 16139371
  15. Ballou LM Dual regulation of glycogen synthase kinase-3beta by the alpha1A-adrenergic receptor. J Biol Chem 2001 276 40910 6 11533051
  16. Barth AM Alpha2-adrenergic receptors modify dendritic spike generation via HCN channels in the prefrontal cortex. J Neurophysiol 2008 99 394 401 18003878
  17. Beaulieu J-M Regulation of Akt signaling by D2 and D3 dopamine receptors in vivo. The Journal of neuroscience 2007 27 881 885 17251429 PMC6672900
  18. Beaulieu JM Lithium antagonizes dopamine-dependent behaviors mediated by an AKT/glycogen synthase kinase 3 signaling cascade. Proc Natl Acad Sci U S A 2004 101 5099 104 15044694 PMC387380
  19. Beaulieu JM An Akt/beta-arrestin 2/PP2A signaling complex mediates dopaminergic neurotransmission and behavior. Cell 2005 122 261 73 16051150
  20. Beaulieu JM Gainetdinov RR The physiology, signaling, and pharmacology of dopamine receptors. Pharmacol Rev 2011 63 182 217 21303898
  21. Bennett BD Huguenard JR Prince DA Adrenergic modulation of GABAA receptor-mediated inhibition in rat sensorimotor cortex. J Neurophysiol 1998 79 937 46 9463454
  22. Bergson C Regional, cellular, and subcellular variations in the distribution of D1 and D5 dopamine receptors in primate brain. J Neurosci 1995 15 7821 36 8613722 PMC6577925
  23. Berridge CW Waterhouse BD The locus coeruleus-noradrenergic system: modulation of behavioral state and state-dependent cognitive processes. Brain Res Brain Res Rev 2003 42 33 84 12668290
  24. Bigham MH Lidow MS Adrenergic and serotonergic receptors in aged monkey neocortex. Neurobiol Aging 1995 16 91 104 7723941
  25. Bijur GN Jope RS Proapoptotic stimuli induce nuclear accumulation of glycogen synthase kinase-3β*. Journal of Biological Chemistry 2001 276 37436 37442 11495916 PMC1973163
  26. Bingham B Early Adolescence as a Critical Window During Which Social Stress Distinctly Alters Behavior and Brain Norepinephrine Activity. Neuropsychopharmacology 2011 36 896 909 21178981 PMC3055730
  27. Blanc G Blockade of prefronto-cortical alpha 1-adrenergic receptors prevents locomotor hyperactivity induced by subcortical D-amphetamine injection. Eur J Neurosci 1994 6 293 8 7912614
  28. Brennan AR Arnsten AF Neuronal mechanisms underlying attention deficit hyperactivity disorder: the influence of arousal on prefrontal cortical function. Ann N Y Acad Sci 2008 1129 236 45 18591484 PMC2863119
  29. Brozoski TJ Cognitive deficit caused by regional depletion of dopamine in prefrontal cortex of rhesus monkey. Science 1979 205 929 32 112679
  30. Cai JX Arnsten AF Dose-dependent effects of the dopamine D1 receptor agonists A77636 or SKF81297 on spatial working memory in aged monkeys. J Pharmacol Exp Ther 1997 283 183 9 9336323
  31. Carr DB alpha2-Noradrenergic receptors activation enhances excitability and synaptic integration in rat prefrontal cortex pyramidal neurons via inhibition of HCN currents. J Physiol 2007 584 437 50 17702809 PMC2277172
  32. Castner SA Williams GV Tuning the engine of cognition: a focus on NMDA/D1 receptor interactions in prefrontal cortex. Brain Cogn 2007 63 94 122 17204357
  33. Cauli B Molecular and physiological diversity of cortical nonpyramidal cells. J Neurosci 1997 17 3894 906 9133407 PMC6573690
  34. Chandler D Waterhouse BD Evidence for broad versus segregated projections from cholinergic and noradrenergic nuclei to functionally and anatomically discrete subregions of prefrontal cortex. Front Behav Neurosci 2012 6 20 22661934 PMC3356860
  35. Chandler DJ Lamperski CS Waterhouse BD Identification and distribution of projections from monoaminergic and cholinergic nuclei to functionally differentiated subregions of prefrontal cortex. Brain Res 2013 1522 38 58 23665053 PMC3811940
  36. Chandler DJ Waterhouse BD Gao W-J New Perspectives on Catecholaminergic Regulation of Executive Circuits: Evidence for Independent Modulation of Prefrontal Functions by Midbrain Dopaminergic and Noradrenergic Neurons. Frontiers in Neural Circuits 2014b 8 53 24904299 PMC4033238
  37. Chen P Glycogen synthase kinase 3 regulates N-methyl-D-aspartate receptor channel trafficking and function in cortical neurons. Molecular pharmacology 2007 72 40 51 17400762
  38. Clark KL Noudoost B The role of prefrontal catecholamines in attention and working memory. Front Neural Circuits 2014 8 33 24782714 PMC3986539
  39. Daniels CR Exogenous ubiquitin modulates chronic beta-adrenergic receptor-stimulated myocardial remodeling: role in Akt activity and matrix metalloproteinase expression. Am J Physiol Heart Circ Physiol 2012 303 H1459 68 23042947 PMC3532534
  40. Darracq L Importance of the noradrenaline-dopamine coupling in the locomotor activating effects of D-amphetamine. J Neurosci 1998 18 2729 39 9502830 PMC6793121
  41. Dawirs RR Teuchert-Noodt G Czaniera R Maturation of the dopamine innervation during postnatal development of the prefrontal cortex in gerbils (Meriones unguiculatus). A quantitative immunocytochemical study. J Hirnforsch 1993 34 281 90 8270782
  42. Dawirs RR Teuchert-Noodt G Czaniera R The postnatal maturation of dopamine innervation in the prefrontal cortex of gerbils (Meriones unguiculatus) is sensitive to an early single dose of methamphetamine. A quantitative immunocytochemical study. J Hirnforsch 1994 35 195 204 8064138
  43. Du J A kinesin signaling complex mediates the ability of GSK-3β to affect mood-associated behaviors. Proceedings of the National Academy of Sciences 2010 107 11573 11578 PMC2895136 20534517
  44. Emamian ES Convergent evidence for impaired AKT1-GSK3beta signaling in schizophrenia. Nat Genet 2004 36 131 7 14745448
  45. Emamian ES AKT/GSK3 signaling pathway and schizophrenia. Front Mol Neurosci 2012 5 33 22435049 PMC3304298
  46. Flores-Hernandez J Dopamine enhancement of NMDA currents in dissociated medium-sized striatal neurons: role of D1 receptors and DARPP-32. J Neurophysiol 2002 88 3010 20 12466426
  47. Forde J.a. Dale TC Glycogen synthase kinase 3: a key regulator of cellular fate. Cellular and molecular life sciences 2007 64 1930 1944 17530463 PMC11136264
  48. Frame S Cohen P GSK3 takes centre stage more than 20 years after its discovery. Biochem. J 2001 359 1 16 11563964 PMC1222116
  49. Franowicz JS Mutation of the alpha2A-adrenoceptor impairs working memory performance and annuls cognitive enhancement by guanfacine. J Neurosci 2002 22 8771 7 12351753 PMC6757781
  50. Gamo NJ Stress impairs prefrontal cortical function via D1 dopamine receptor interactions with hyperpolarization-activated cyclic nucleotide-gated channels. Biol Psychiatry 2015 PMC4524795 25731884
  51. Gao WJ Goldman-Rakic PS Selective modulation of excitatory and inhibitory microcircuits by dopamine. Proc Natl Acad Sci U S A 2003 100 2836 41 12591942 PMC151427
  52. George SA Altered locus coeruleus-norepinephrine function following single prolonged stress. Eur J Neurosci 2013 37 901 9 23279008
  53. Gioanni Y Alpha1-adrenergic, D1, and D2 receptors interactions in the prefrontal cortex: implications for the modality of action of different types of neuroleptics. Synapse 1998 30 362 70 9826228
  54. Giros B Delineation of discrete domains for substrate, cocaine, and tricyclic antidepressant interactions using chimeric dopamine-norepinephrine transporters. J Biol Chem 1994 269 15985 8 8206893
  55. Goldman-Rakic PS Lidow MS Gallager DW Overlap of dopaminergic, adrenergic, and serotoninergic receptors and complementarity of their subtypes in primate prefrontal cortex. J Neurosci 1990 10 2125 38 2165520 PMC6570394
  56. Gonzalez-Burgos G Dopaminergic modulation of short-term synaptic plasticity in fast-spiking interneurons of primate dorsolateral prefrontal cortex. J Neurophysiol 2005 94 4168 4177 16148267
  57. Gonzalez-Islas C Hablitz JJ Dopamine inhibition of evoked IPSCs in rat prefrontal cortex. J Neurophysiol 2001 86 2911 8 11731547
  58. Gonzalez-Islas C Hablitz JJ Dopamine enhances EPSCs in layer II-III pyramidal neurons in rat prefrontal cortex. J Neurosci 2003 23 867 75 12574415 PMC6741914
  59. Goto Y Grace AA The dopamine system and the pathophysiology of schizophrenia: a basic science perspective. Int Rev Neurobiol 2007 78 41 68 17349857
  60. Goto Y Yang CR Otani S Functional and dysfunctional synaptic plasticity in prefrontal cortex: roles in psychiatric disorders. Biol Psychiatry 2010 67 199 207 19833323
  61. Gould TD Manji HK Glycogen synthase kinase-3: a putative molecular target for lithium mimetic drugs. Neuropsychopharmacology 2005 30 1223 1237 15827567
  62. Granon S Enhanced and impaired attentional performance after infusion of D1 dopaminergic receptor agents into rat prefrontal cortex. J Neurosci 2000 20 1208 15 10648725 PMC6774157
  63. Graziane NM Yuen EY Yan Z Dopamine D4 Receptors Regulate GABAA Receptor Trafficking via an Actin/Cofilin/Myosin-dependent Mechanism. J Biol Chem 2009 284 8329 36 19179335 PMC2659191
  64. Gu H Wall SC Rudnick G Stable expression of biogenic amine transporters reveals differences in inhibitor sensitivity, kinetics, and ion dependence. J Biol Chem 1994 269 7124 30 8125921
  65. Hara M Role of adrenoceptors in the regulation of dopamine/DARPP-32 signaling in neostriatal neurons. J Neurochem 2010 113 1046 59 20236221 PMC2861145
  66. Hernandez-Lopez S D2 dopamine receptors in striatal medium spiny neurons reduce L-type Ca2+ currents and excitability via a novel PLC[beta]1-IP3-calcineurin-signaling cascade. J Neurosci 2000 20 8987 95 11124974 PMC6773013
  67. Hieble JP International Union of Pharmacology. X. Recommendation for nomenclature of alpha 1-adrenoceptors: consensus update. Pharmacol Rev 1995 47 267 70 7568329
  68. Hopkins WF Johnston D Frequency-dependent noradrenergic modulation of long-term potentiation in the hippocampus. Science 1984 226 350 2 6091272
  69. Hu J-L Dopamine D1 receptor-mediated NMDA receptor insertion depends on Fyn but not Src kinase pathway in prefrontal cortical neurons. Molecular Brain 2010 3 1 14 20569495 PMC2902469
  70. Jakala P Guanfacine and clonidine, alpha 2-agonists, improve paired associates learning, but not delayed matching to sample, in humans. Neuropsychopharmacology 1999 20 119 30 9885792
  71. Jay TM Dopamine: a potential substrate for synaptic plasticity and memory mechanisms. Prog Neurobiol 2003 69 375 90 12880632
  72. Johnson G Comparative effects of lithium and chlorpromazine in the treatment of acute manic states. The British Journal of Psychiatry 1971 119 267 276 4936131
  73. Kandel ER Principles of neural science 2013 McGraw-Hill New York
  74. Katsuki H Izumi Y Zorumski CF Noradrenergic regulation of synaptic plasticity in the hippocampal CA1 region. J Neurophysiol 1997 77 3013 20 9212253
  75. Kawaguchi Y Physiological subgroups of nonpyramidal cells with specific morphological characteristics in layer II/III of rat frontal cortex. J Neurosci 1995 15 2638 55 7722619 PMC6577784
  76. Kawaguchi Y Shindou T Noradrenergic excitation and inhibition of GABAergic cell types in rat frontal cortex. J Neurosci 1998 18 6963 76 9712665 PMC6792977
  77. Khan ZU Differential regional and cellular distribution of dopamine D2-like receptors: an immunocytochemical study of subtype-specific antibodies in rat and human brain. J Comp Neurol 1998 402 353 71 9853904
  78. Klein PS Melton DA A molecular mechanism for the effect of lithium on development. Proc Natl Acad Sci U S A 1996 93 8455 9 8710892 PMC38692
  79. Knable MB Weinberger DR Dopamine, the prefrontal cortex and schizophrenia. J Psychopharmacol 1997 11 123 31 9208376
  80. Kobayashi M Differential regulation of synaptic transmission by adrenergic agonists via protein kinase A and protein kinase C in layer V pyramidal neurons of rat cerebral cortex. Neuroscience 2007 146 1772 84 17478051
  81. Kobayashi M Presynaptic and postsynaptic modulation of glutamatergic synaptic transmission by activation of alpha(1)- and beta-adrenoceptors in layer V pyramidal neurons of rat cerebral cortex. Synapse 2009 63 269 81 19116948
  82. Krause B Marquez-Ruiz J Cohen Kadosh R The effect of transcranial direct current stimulation: a role for cortical excitation/inhibition balance? Front Hum Neurosci 2013 7 602 24068995 PMC3781319
  83. Kroner S Dopamine increases inhibition in the monkey dorsolateral prefrontal cortex through cell type-specific modulation of interneurons. Cereb Cortex 2007 17 1020 32 16772311
  84. Lambe EK Krimer LS Goldman-Rakic PS Differential postnatal development of catecholamine and serotonin inputs to identified neurons in prefrontal cortex of rhesus monkey. J Neurosci 2000 20 8780 7 11102486 PMC6773090
  85. Lammel S Unique properties of mesoprefrontal neurons within a dual mesocorticolimbic dopamine system. Neuron 2008 57 760 73 18341995
  86. Lammel S Input-specific control of reward and aversion in the ventral tegmental area. Nature 2012 491 212 7 23064228 PMC3493743
  87. Lammel S Diversity of transgenic mouse models for selective targeting of midbrain dopamine neurons. Neuron 2015 85 429 38 25611513 PMC5037114
  88. Lapiz MD Morilak DA Noradrenergic modulation of cognitive function in rat medial prefrontal cortex as measured by attentional set shifting capability. Neuroscience 2006 137 1039 49 16298081
  89. Latsari M Noradrenergic innervation of the developing and mature visual and motor cortex of the rat brain: a light and electron microscopic immunocytochemical analysis. J Comp Neurol 2002 445 145 58 11891659
  90. Law-Tho D Hirsch JC Crepel F Dopamine modulation of synaptic transmission in rat prefrontal cortex: an in vitro electrophysiological study. Neurosci Res 1994 21 151 60 7724066
  91. Le Magueresse C Monyer H GABAergic Interneurons Shape the Functional Maturation of the Cortex. Neuron 2013 77 388 405 23395369
  92. Leslie CA Postnatal development of D1 dopamine receptors in the medial prefrontal cortex, striatum and nucleus accumbens of normal and neonatal 6-hydroxydopamine treated rats: a quantitative autoradiographic analysis. Brain Res Dev Brain Res 1991 62 109 14 1836980
  93. Levitt P Moore RY Development of the noradrenergic innervation of neocortex. Brain Res 1979 162 243 59 761089
  94. Levy F Dopamine vs noradrenaline: inverted-U effects and ADHD theories. Aust N Z J Psychiatry 2009 43 101 8 19153917
  95. Lewis DA Morrison JH Noradrenergic innervation of monkey prefrontal cortex: a dopamine-beta-hydroxylase immunohistochemical study. J Comp Neurol 1989 282 317 30 2715385
  96. Lewis DA The catecholaminergic innervation of primate prefrontal cortex. J Neural Transm Suppl 1992 36 179 200 1527517
  97. Lewis DA Dopamine transporter immunoreactivity in monkey cerebral cortex: regional, laminar, and ultrastructural localization. J Comp Neurol 2001 432 119 36 11241381
  98. Li BM Alpha-2 adrenergic modulation of prefrontal cortical neuronal activity related to spatial working memory in monkeys. Neuropsychopharmacology 1999 21 601 10 10516956
  99. Li Q Sarna SK Chronic stress targets posttranscriptional mechanisms to rapidly upregulate alpha1C-subunit of Cav1.2b calcium channels in colonic smooth muscle cells. Am J Physiol Gastrointest Liver Physiol 2011 300 G154 63 21051529 PMC3025508
  100. Li YC Activation of glycogen synthase kinase-3 beta is required for hyperdopamine and D2 receptor-mediated inhibition of synaptic NMDA receptor function in the rat prefrontal cortex. J Neurosci 2009 29 15551 63 20007479 PMC2832219
  101. Li YC Gao WJ GSK-3beta activity and hyperdopamine-dependent behaviors. Neurosci Biobehav Rev 2011 35 645 654 20727368 PMC2997336
  102. Li YC Wang MJ Gao WJ Hyperdopaminergic modulation of inhibitory transmission is dependent on GSK-3beta signaling-mediated trafficking of GABA(A) receptors. J Neurochem 2012 PMC3443500 22676038
  103. Lim EP Locus coeruleus stimulation and noradrenergic modulation of hippocampo-prefrontal cortex long-term potentiation. Int J Neuropsychopharmacol 2010 13 1219 31 20128952
  104. Lin YW Enhancement of associative long-term potentiation by activation of beta-adrenergic receptors at CA1 synapses in rat hippocampal slices. J Neurosci 2003 23 4173 81 12764105 PMC6741099
  105. Lisman J Excitation, inhibition, local oscillations, or large-scale loops: what causes the symptoms of schizophrenia? Curr Opin Neurobiol 2012 22 537 44 22079494 PMC3302967
  106. Liu W Adrenergic modulation of NMDA receptors in prefrontal cortex is differentially regulated by RGS proteins and spinophilin. Proc Natl Acad Sci U S A 2006 103 18338 43 17101972 PMC1838752
  107. Liu Y Expression of beta1- and beta2-adrenoceptors in different subtypes of interneurons in the medial prefrontal cortex of mice. Neuroscience 2014 257 149 57 24215978
  108. Luo F Activation of alpha(1)-adrenoceptors enhances excitatory synaptic transmission via a pre- and postsynaptic protein kinase C-dependent mechanism in the medial prefrontal cortex of rats. Eur J Neurosci 2014 39 1281 93 24494713
  109. Luo L Callaway EM Svoboda K Genetic dissection of neural circuits. Neuron 2008 57 634 60 18341986 PMC2628815
  110. MacDonald E Kobilka BK Scheinin M Gene targeting--homing in on alpha 2-adrenoceptor-subtype function. Trends Pharmacol Sci 1997 18 211 9 9227000
  111. Mao Y Disrupted in schizophrenia 1 regulates neuronal progenitor proliferation via modulation of GSK3beta/beta-catenin signaling. Cell 2009 136 1017 31 19303846 PMC2704382
  112. Marek GJ Aghajanian GK 5-HT2A receptor or alpha1-adrenoceptor activation induces excitatory postsynaptic currents in layer V pyramidal cells of the medial prefrontal cortex. Eur J Pharmacol 1999 367 197 206 10078993
  113. Masana MI Lithium effects on noradrenergic-linked adenylate cyclase activity in intact rat brain: an in vivo microdialysis study. Brain Res 1991 538 333 6 1849439
  114. Menon B Glycogen synthase kinase-3beta plays a pro-apoptotic role in beta-adrenergic receptor-stimulated apoptosis in adult rat ventricular myocytes: Role of beta1 integrins. J Mol Cell Cardiol 2007 42 653 61 17292911 PMC1894917
  115. Missale C Dopamine receptors: from structure to function. Physiol Rev 1998 78 189 225 9457173
  116. Missale C The neurobiology of dopamine receptors: evolution from the dual concept to heterodimer complexes. J Recept Signal Transduct Res 2010 30 347 54 20684667
  117. Mitrano DA D1-dopamine and alpha1-adrenergic receptors co-localize in dendrites of the rat prefrontal cortex. Neuroscience 2014 258 90 100 24231738 PMC3913162
  118. Moll GH Heinrich H Rothenberger A Methylphenidate and intracortical excitability: opposite effects in healthy subjects and attention-deficit hyperactivity disorder. Acta Psychiatr Scand 2003 107 69 72 12558545
  119. Montezinho LP The interaction between dopamine D2-like and beta-adrenergic receptors in the prefrontal cortex is altered by mood-stabilizing agents. J Neurochem 2006 96 1336 48 16478526
  120. Monyer H Markram H Interneuron Diversity series: Molecular and genetic tools to study GABAergic interneuron diversity and function. Trends Neurosci 2004 27 90 7 15102488
  121. Morilak DA Role of brain norepinephrine in the behavioral response to stress. Prog Neuropsychopharmacol Biol Psychiatry 2005 29 1214 24 16226365
  122. Morioka N A beta1/2 adrenergic receptor-sensitive intracellular signaling pathway modulates CCL2 production in cultured spinal astrocytes. J Cell Physiol 2014 229 323 32 24037783
  123. Morisco C The Akt-glycogen synthase kinase 3beta pathway regulates transcription of atrial natriuretic factor induced by beta-adrenergic receptor stimulation in cardiac myocytes. J Biol Chem 2000 275 14466 75 10799529
  124. Moron JA Dopamine uptake through the norepinephrine transporter in brain regions with low levels of the dopamine transporter: evidence from knock-out mouse lines. J Neurosci 2002 22 389 95 11784783 PMC6758674
  125. Moule SK Regulation of Protein Kinase B and Glycogen Synthase Kinase-3 by Insulin and β-Adrenergic Agonists in Rat Epididymal Fat Cells: ACTIVATION OF PROTEIN KINASE B BY WORTMANNIN-SENSITIVE AND -INSENSITIVE MECHANISMS. Journal of Biological Chemistry 1997 272 7713 7719 9065430
  126. Mrzljak L Localization of dopamine D4 receptors in GABAergic neurons of the primate brain. Nature 1996 381 245 8 8622768
  127. Murphy BL Dopamine and spatial working memory in rats and monkeys: pharmacological reversal of stress-induced impairment. J Neurosci 1996 16 7768 75 8922432 PMC6579090
  128. Niwa M Adolescent stress–induced epigenetic control of dopaminergic neurons via glucocorticoids. Science 2013 339 335 339 23329051 PMC3617477
  129. Nomura S Noradrenalin and dopamine receptors both control cAMP-PKA signaling throughout the cerebral cortex. Front Cell Neurosci 2014 8 247 25191229 PMC4140213
  130. O'Brien WT Glycogen synthase kinase-3beta haploinsufficiency mimics the behavioral and molecular effects of lithium. J Neurosci 2004 24 6791 8 15282284 PMC5328671
  131. Oh SW A mesoscale connectome of the mouse brain. Nature 2014 508 207 14 24695228 PMC5102064
  132. Onn SP Dopamine D1 and D4 receptor subtypes differentially modulate recurrent excitatory synapses in prefrontal cortical pyramidal neurons. Neuropsychopharmacology 2006 31 318 38 16052247
  133. Pascucci T The medial prefrontal cortex determines the accumbens dopamine response to stress through the opposing influences of norepinephrine and dopamine. Cereb Cortex 2007 17 2796 804 17322559
  134. Paspalas CD Goldman-Rakic PS Presynaptic d1 dopamine receptors in primate prefrontal cortex: target-specific expression in the glutamatergic synapse. J Neurosci 2005 25 1260 7 15689564 PMC6725972
  135. Peineau S.p. The role of GSK-3 in synaptic plasticity. British journal of pharmacology 2008 153 S428 S437 18311157 PMC2268071
  136. Penit-Soria J Audinat E Crepel F Excitation of rat prefrontal cortical neurons by dopamine: an in vitro electrophysiological study. Brain Res 1987 425 263 74 3427429
  137. Perova Z Delevich K Li B Depression of excitatory synapses onto parvalbumin interneurons in the medial prefrontal cortex in susceptibility to stress. J Neurosci 2015 35 3201 6 25698754 PMC4331634
  138. Pouget P A fragile balance: perturbation of GABA mediated circuit in prefrontal cortex generates high intraindividual performance variability. PLoS One 2009 4 e5208 19381296 PMC2668174
  139. Puig MV Dopamine modulation of learning and memory in the prefrontal cortex: insights from studies in primates, rodents, and birds. Front Neural Circuits 2014 8 93 25140130 PMC4122189
  140. Qian H beta2-Adrenergic receptor supports prolonged theta tetanus-induced LTP. J Neurophysiol 2012 107 2703 12 22338020 PMC3362273
  141. Rainbow TC Parsons B Wolfe BB Quantitative autoradiography of beta 1- and beta 2-adrenergic receptors in rat brain. Proc Natl Acad Sci U S A 1984 81 1585 9 6324206 PMC344882
  142. Raman IM Tong G Jahr CE Beta-adrenergic regulation of synaptic NMDA receptors by cAMP-dependent protein kinase. Neuron 1996 16 415 21 8789956
  143. Ramos BP Arnsten AF Adrenergic pharmacology and cognition: focus on the prefrontal cortex. Pharmacol Ther 2007 113 523 36 17303246 PMC2151919
  144. Robertson SD Insulin reveals Akt signaling as a novel regulator of norepinephrine transporter trafficking and norepinephrine homeostasis. J Neurosci 2010 30 11305 16 20739551 PMC3448453
  145. Roh MS Haloperidol and clozapine differentially regulate signals upstream of glycogen synthase kinase 3 in the rat frontal cortex. Exp Mol Med 2007 39 353 60 17603289
  146. Rossetti ZL Carboni S Noradrenaline and dopamine elevations in the rat prefrontal cortex in spatial working memory. J Neurosci 2005 25 2322 9 15745958 PMC6726105
  147. Roychowdhury S Layer- and area-specificity of the adrenergic modulation of synaptic transmission in the rat neocortex. Neurochem Res 2014 39 2377 84 25266551
  148. Santana N Mengod G Artigas F Quantitative analysis of the expression of dopamine D1 and D2 receptors in pyramidal and GABAergic neurons of the rat prefrontal cortex. Cereb Cortex 2009 19 849 60 18689859
  149. Sawaguchi T Matsumura M Kubota K Dopamine enhances the neuronal activity of spatial short-term memory task in the primate prefrontal cortex. Neurosci Res 1988 5 465 73 3399149
  150. Sawaguchi T Matsumura M Kubota K Catecholaminergic effects on neuronal activity related to a delayed response task in monkey prefrontal cortex. J Neurophysiol 1990 63 1385 400 2358882
  151. Sawaguchi T Goldman-Rakic PS The role of D1-dopamine receptor in working memory: local injections of dopamine antagonists into the prefrontal cortex of rhesus monkeys performing an oculomotor delayed-response task. J Neurophysiol 1994 71 515 28 7909839
  152. Scheid MP Woodgett JR PKB/AKT: functional insights from genetic models. Nature Reviews Molecular Cell Biology 2001 2 760 768 11584303
  153. Schmeichel BE Berridge CW Neurocircuitry Underlying the Preferential Sensitivity of Prefrontal Catecholamines to Low-Dose Psychostimulants. Neuropsychopharmacology 2013 38 1078 1084 23303075 PMC3629407
  154. Schmeichel BE Zemlan FP Berridge CW A selective dopamine reuptake inhibitor improves prefrontal cortex-dependent cognitive function: Potential relevance to attention deficit hyperactivity disorder. Neuropharmacology 2013 64 321 328 22796428 PMC3445755
  155. Seamans JK Dopamine D1/D5 receptor modulation of excitatory synaptic inputs to layer V prefrontal cortex neurons. Proc Natl Acad Sci U S A 2001a 98 301 6 11134516 PMC14585
  156. Seamans JK Bidirectional dopamine modulation of GABAergic inhibition in prefrontal cortical pyramidal neurons. J Neurosci 2001b 21 3628 38 11331392 PMC6762481
  157. Seamans JK Yang CR The principal features and mechanisms of dopamine modulation in the prefrontal cortex. Prog Neurobiol 2004 74 1 58 15381316
  158. Sesack SR Dopamine axon varicosities in the prelimbic division of the rat prefrontal cortex exhibit sparse immunoreactivity for the dopamine transporter. J Neurosci 1998 18 2697 708 9502827 PMC6793120
  159. Shi WX Characterization of dopamine-induced depolarization of prefrontal cortical neurons. Synapse 1997 26 415 22 9215600
  160. Silberberg G Synaptic pathways in neural microcircuits. Trends in Neurosciences 2005 28 541 551 16122815
  161. Singh M Extracellular ubiquitin inhibits beta-AR-stimulated apoptosis in cardiac myocytes: role of GSK-3beta and mitochondrial pathways. Cardiovasc Res 2010 86 20 8 20015977 PMC2836259
  162. Siuta MA Dysregulation of the norepinephrine transporter sustains cortical hypodopaminergia and schizophrenia-like behaviors in neuronal rictor null mice. PLoS Biol 2010 8 e1000393 20543991 PMC2882427
  163. Spear LP The adolescent brain and age-related behavioral manifestations. Neurosci Biobehav Rev 2000 24 417 463 10817843
  164. Spencer RC Klein RM Berridge CW Psychostimulants act within the prefrontal cortex to improve cognitive function. Biol Psychiatry 2012 72 221 227 22209638 PMC3319517
  165. Stanton PK Sarvey JM Depletion of norepinephrine, but not serotonin, reduces long-term potentiation in the dentate gyrus of rat hippocampal slices. J Neurosci 1985 5 2169 76 4040556 PMC6565305
  166. Summers RJ Expression of beta 3-adrenoceptor mRNA in rat brain. Br J Pharmacol 1995 116 2547 8 8590968 PMC1909119
  167. Sutton L Rushlow W The effects of neuropsychiatric drugs on glycogen synthase kinase-3 signaling. Neuroscience 199 116 124 22001305
  168. Taghzouti K Behavioural deficits induced by an electrolytic lesion of the rat ventral mesencephalic tegmentum are corrected by a superimposed lesion of the dorsal noradrenergic system. Brain Res 1988 440 172 6 3129124
  169. Tanila H Rama P Carlson S The effects of prefrontal intracortical microinjections of an alpha-2 agonist, alpha-2 antagonist and lidocaine on the delayed alternation performance of aged rats. Brain Res Bull 1996 40 117 9 8724429
  170. Tassin JP Norepinephrine-dopamine interactions in the prefrontal cortex and the ventral tegmental area: relevance to mental diseases. Adv Pharmacol 1998 42 712 6 9327998
  171. Tenorio G 'Silent' priming of translation-dependent LTP by ss-adrenergic receptors involves phosphorylation and recruitment of AMPA receptors. Learn Mem 2010 17 627 38 21097606 PMC2998333
  172. Thompson JL Pogue-Geile MF Grace AA Developmental pathology, dopamine, and stress: a model for the age of onset of schizophrenia symptoms. Schizophr Bull 2004 30 875 900 15954196
  173. Thuault SJ Prefrontal cortex HCN1 channels enable intrinsic persistent neural firing and executive memory function. J Neurosci 2013 33 13583 99 23966682 PMC3755709
  174. Towers SK Hestrin S D1-like dopamine receptor activation modulates GABAergic inhibition but not electrical coupling between neocortical fast-spiking interneurons. J Neurosci 2008 28 2633 41 18322106 PMC4191929
  175. Trantham-Davidson H Mechanisms underlying differential D1 versus D2 dopamine receptor regulation of inhibition in prefrontal cortex. J Neurosci 2004 24 10652 9 15564581 PMC5509068
  176. Tritsch NX Sabatini BL Dopaminergic modulation of synaptic transmission in cortex and striatum. Neuron 2012 76 33 50 23040805 PMC4386589
  177. Tseng KY O'Donnell P Dopamine modulation of prefrontal cortical interneurons changes during adolescence. Cereb Cortex 2007 17 1235 40 16818475 PMC2204087
  178. Tully K Norepinephrine enables the induction of associative long-term potentiation at thalamo-amygdala synapses. Proc Natl Acad Sci U S A 2007 104 14146 50 17709755 PMC1955781
  179. Urban KR Waterhouse BD Gao WJ Distinct age-dependent effects of methylphenidate on developing and adult prefrontal neurons. Biol Psychiatry 2012 72 880 888 22609367 PMC3433628
  180. Urban KR Li YC Gao WJ Treatment with a clinically-relevant dose of methylphenidate alters NMDA receptor composition and synaptic plasticity in the juvenile rat prefrontal cortex. Neurobiol Learn Mem 2013 101 65 74 23333502 PMC3602399
  181. Urban NN Selective reduction by dopamine of excitatory synaptic inputs to pyramidal neurons in primate prefrontal cortex. J Physiol 2002 539 707 12 11897842 PMC2290171
  182. Ventura R Norepinephrine in the prefrontal cortex is critical for amphetamine-induced reward and mesoaccumbens dopamine release. J Neurosci 2003 23 1879 85 12629192 PMC6741949
  183. Ventura R Alcaro A Puglisi-Allegra S Prefrontal cortical norepinephrine release is critical for morphine-induced reward, reinstatement and dopamine release in the nucleus accumbens. Cereb Cortex 2005 15 1877 86 15728739
  184. Ventura R Morrone C Puglisi-Allegra S Prefrontal/accumbal catecholamine system determines motivational salience attribution to both reward- and aversion-related stimuli. Proc Natl Acad Sci U S A 2007 104 5181 6 17360372 PMC1820518
  185. Ventura R Postnatal aversive experience impairs sensitivity to natural rewards and increases susceptibility to negative events in adult life. Cereb Cortex 2013 23 1606 17 22669969
  186. Vezina P Opposed Behavioural Outputs of Increased Dopamine Transmission in Prefrontocortical and Subcortical Areas: A Role for the Cortical D-1 Dopamine Receptor. Eur J Neurosci 1991 3 1001 1007 12106258
  187. Vincent SL Khan Y Benes FM Cellular distribution of dopamine D1 and D2 receptors in rat medial prefrontal cortex. J Neurosci 1993 13 2551 64 8501521 PMC6576493
  188. Wang HX Waterhouse BD Gao WJ Selective suppression of excitatory synapses on GABAergic interneurons by norepinephrine in juvenile rat prefrontal cortical microcircuitry. Neuroscience 2013 246 312 28 23684615 PMC3697018
  189. Wang X Zhong P Yan Z Dopamine D4 receptors modulate GABAergic signaling in pyramidal neurons of prefrontal cortex. J Neurosci 2002 22 9185 93 12417643 PMC6758062
  190. Wei J Liu W Yan Z Regulation of AMPA receptor trafficking and function by glycogen synthase kinase 3. J Biol Chem 2010 285 26369 76 20584904 PMC2924064
  191. Williams GV Castner SA Under the curve: critical issues for elucidating D1 receptor function in working memory. Neuroscience 2006 139 263 76 16310964
  192. Winterer G Weinberger DR Genes, dopamine and cortical signal-to-noise ratio in schizophrenia. Trends Neurosci 2004 27 683 90 15474169
  193. Xu TX Yao WD D1 and D2 dopamine receptors in separate circuits cooperate to drive associative long-term potentiation in the prefrontal cortex. Proc Natl Acad Sci U S A 2010 107 16366 71 20805489 PMC2941310
  194. Yang CR Seamans JK Dopamine D1 receptor actions in layers V-VI rat prefrontal cortex neurons in vitro: modulation of dendritic-somatic signal integration. J Neurosci 1996 16 1922 35 8774459 PMC6578685
  195. Yi F Signaling mechanism underlying alpha2A -adrenergic suppression of excitatory synaptic transmission in the medial prefrontal cortex of rats. Eur J Neurosci 2013 38 2364 73 23701442
  196. Yizhar O Neocortical excitation/inhibition balance in information processing and social dysfunction. Nature 2011 477 171 8 21796121 PMC4155501
  197. Zahrt J Supranormal stimulation of D1 dopamine receptors in the rodent prefrontal cortex impairs spatial working memory performance. J Neurosci 1997 17 8528 35 9334425 PMC6573725
  198. Zhang W beta-Adrenergic receptor-PI3K signaling crosstalk in mouse heart: elucidation of immediate downstream signaling cascades. PLoS One 2011 6 e26581 22028912 PMC3197531
  199. Zhou FM Hablitz JJ Dopamine modulation of membrane and synaptic properties of interneurons in rat cerebral cortex. J Neurophysiol 1999 81 967 76 10085325
  200. Zhou HC Activation of beta2-adrenoceptor enhances synaptic potentiation and behavioral memory via cAMP-PKA signaling in the medial prefrontal cortex of rats. Learn Mem 2013 20 274 84 23596314

Cited by

Sorted by citations

Authors
Xing, B., Li, Y.-C., & Gao, W.-J.
Affiliations
Drexel University (US)
Corresponding author
Gao, Wen-Jun
Venue
Brain Research
Publisher
Elsevier BV
Published
2016-06
Volume
1641
Issue
Pt B
Pages
217-233
ISSN
0006-8993 (ISSN-L)
OpenAlex
W2234486753
Cited by
196
References
29
Citations by year
2026: 16 · 2025: 32 · 2024: 17 · 2023: 16 · 2022: 26 · 2021: 27 · 2020: 22 · 2019: 14 · 2018: 10 · 2017: 11 · 2016: 5
FWCI
1.46
Type
journal article
Language
en
Open access
Locations
  • Brain Research (publishedVersion)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion)
  • PubMed Central (acceptedVersion)
Funders
NIH (R01MH085666, R03MH101578)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
Keywords
norepinephrine, dopamine, prefrontal cortex, synaptic modulation, catecholamines, neuromodulation, synaptic integration, receptor signaling pathways, noradrenergic system, working memory, attention, neuropsychiatric disorders
MeSH terms
Animals, Dopamine, Humans, Synaptic Transmission, Norepinephrine, Synapses, Prefrontal Cortex

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