Noradrenaline transporter blockade increases fronto-parietal functional connectivity relevant for working memory

European Neuropsychopharmacology

Volumn 27, Issue 4, 2017, Pages 399-410

  Hernaus, Dennis ^a   Casales Santa, Marta M ^b   Offermann, Jan Stefan ^b   Van Amelsvoort, Thérèse ^b  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b MAASTRICHT UNIVERSITY   (Netherlands)

Author keywords

Cognition; Dopamine; FMRI; Noradrenaline; Prefrontal cortex; Working memory

Indexed keywords

ATOMOXETINE; CATECHOLAMINE; ADRENERGIC RECEPTOR AFFECTING AGENT; OXYGEN;

ADULT; ANTERIOR INSULA; ARTICLE; CONTROLLED STUDY; CROSSOVER PROCEDURE; DOUBLE BLIND PROCEDURE; DRUG EFFECT; EXECUTIVE FUNCTION; FRONTO PARIETAL FUNCTIONAL CONNECTIVITY; FRONTOPARIETAL CORTEX; FUNCTIONAL CONNECTIVITY; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL NEUROIMAGING; HUMAN; MALE; MENTAL TASK; N BACK TASK; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE SCANNER; POSTERIOR PARIETAL CORTEX; PRECUNEUS; PRIMARY MOTOR CORTEX; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL; REACTION TIME; SINGLE DRUG DOSE; TASK POSITIVE NETWORK; WORKING MEMORY; ADOLESCENT; BLOOD; BRAIN CORTEX; BRAIN MAPPING; DIAGNOSTIC IMAGING; DRUG EFFECTS; HEMISPHERIC DOMINANCE; IMAGE PROCESSING; METABOLISM; NERVE CELL NETWORK; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY; SHORT TERM MEMORY; YOUNG ADULT;

ADOLESCENT; ADRENERGIC UPTAKE INHIBITORS; ADULT; ATOMOXETINE HYDROCHLORIDE; BRAIN MAPPING; CEREBRAL CORTEX; CROSS-OVER STUDIES; DOUBLE-BLIND METHOD; FUNCTIONAL LATERALITY; HEALTHY VOLUNTEERS; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; MEMORY, SHORT-TERM; NERVE NET; OXYGEN; REACTION TIME; YOUNG ADULT;

EID: 85014780227     PISSN: 0924977X     EISSN: 18737862     Source Type: Journal    
DOI: 10.1016/j.euroneuro.2017.02.004     Document Type: Article

References (65)

1. Aalto, S., Bruck, A., Laine, M., Nagren, K., Rinne, J.O., Frontal and temporal dopamine release during working memory and attention tasks in healthy humans: a positron emission tomography study using the high-affinity dopamine D2 receptor ligand [11C]FLB 457. J. Neurosci. 25:10 (2005), 2471–2477.
2. Arnsten, A.F., Catecholamine influences on dorsolateral prefrontal cortical networks. Biol. Psychiatry 69:12 (2011), e89–e99.
3. Bloemendaal, M., van Schouwenburg, M.R., Miyakawa, A., Aarts, E., D׳Esposito, M., Cools, R., Dopaminergic modulation of distracter-resistance and prefrontal delay period signal. Psychopharmacology 232:6 (2015), 1061–1070.
4. Borchert, R.J., Rittman, T., Passamonti, L., Ye, Z., Sami, S., Jones, S.P., et al. Atomoxetine enhances connectivity of prefrontal networks in Parkinson׳s disease. Neuropsychopharmacol.: Off. Publ. Am. Coll. Neuropsychopharmacol., 41(8), 2016, 2188.
5. Brett, M., Anton, J., Valabregue, R., Poline, J. 2002. (June 2–6). Region of interest analysis using an SPM toolbox Presented at In: Proceedings of the 8th International Conference on Functional Mapping of the Human Brain. Sendai, Japan: Sendai, Japan.
6. Bush, G., Holmes, J., Shin, L.M., Surman, C., Makris, N., Mick, E., et al. Atomoxetine increases fronto-parietal functional MRI activation in attention-deficit/hyperactivity disorder: a pilot study. Psychiatry Res. 211:1 (2013), 88–91.
7. Bymaster, F.P., Katner, J.S., Nelson, D.L., Hemrick-Luecke, S.K., Threlkeld, P.G., Heiligenstein, J.H., et al. Atomoxetine increases extracellular levels of norepinephrine and dopamine in prefrontal cortex of rat: a potential mechanism for efficacy in attention deficit/hyperactivity disorder. Neuropsychopharmacol.: Off. Publ. Am. Coll. Neuropsychopharmacol. 27:5 (2002), 699–711.
8. Cai, W., Ryali, S., Chen, T., Li, C.S., Menon, V., Dissociable roles of right inferior frontal cortex and anterior insula in inhibitory control: evidence from intrinsic and task-related functional parcellation, connectivity, and response profile analyses across multiple datasets. J. Neurosci. 34:44 (2014), 14652–14667.
9. Cole, D.M., Oei, N.Y., Soeter, R.P., Both, S., van Gerven, J.M., Rombouts, S.A., et al. Dopamine-dependent architecture of cortico-subcortical network connectivity. Cereb. Cortex 23:7 (2013), 1509–1516.
10. Cools, R., Frank, M.J., Gibbs, S.E., Miyakawa, A., Jagust, W., D׳Esposito, M., Striatal dopamine predicts outcome-specific reversal learning and its sensitivity to dopaminergic drug administration. J. Neurosci. 29:5 (2009), 1538–1543.
11. Cools, R., Gibbs, S.E., Miyakawa, A., Jagust, W., D׳Esposito, M., Working memory capacity predicts dopamine synthesis capacity in the human striatum. J. Neurosci. 28:5 (2008), 1208–1212.
12. Cubillo, A., Smith, A.B., Barrett, N., Giampietro, V., Brammer, M., Simmons, A., et al. Drug-specific laterality effects on frontal lobe activation of atomoxetine and methylphenidate in attention deficit hyperactivity disorder boys during working memory. Psychol. Med. 44:3 (2014), 633–646.
13. Ding, Y.S., Naganawa, M., Gallezot, J.D., Nabulsi, N., Lin, S.F., Ropchan, J., et al. Clinical doses of atomoxetine significantly occupy both norepinephrine and serotonin transports: implications on treatment of depression and ADHD. NeuroImage 86 (2014), 164–171.
14. Dolphin, A., Jenner, P., Marsden, C.D., Noradrenaline synthesis from L-DOPA in rodents and its relationship to motor activity. Pharmacol., Biochem., Behav. 5:4 (1976), 431–439.
15. Everett, G.M., Borcherding, J.W., L-DOPA: effect on concentrations of dopamine, norepinephrine, and serotonin in brains of mice. Science 168:3933 (1970), 847–850.
16. Gamo, N.J., Wang, M., Arnsten, A.F., Methylphenidate and atomoxetine enhance prefrontal function through alpha2-adrenergic and dopamine D1 receptors. J. Am. Acad. Child Adolesc. Psychiatry 49:10 (2010), 1011–1023.
17. Garrett, D.D., Nagel, I.E., Preuschhof, C., Burzynska, A.Z., Marchner, J., Wiegert, S., et al. Amphetamine modulates brain signal variability and working memory in younger and older adults. Proc. Natl. Acad. Sci. U. S. A. 112:24 (2015), 7593–7598.
18. Gelao, B., Fazio, L., Selvaggi, P., Di Giorgio, A., Taurisano, P., Quarto, T., et al. DRD2 genotype predicts prefrontal activity during working memory after stimulation of D2 receptors with bromocriptine. Psychopharmacology 231:11 (2014), 2361–2370.
19. Gevins, A., Cutillo, B., Spatiotemporal dynamics of component processes in human working memory. Electroencephalogr. Clin. Neurophysiol. 87:3 (1993), 128–143.
20. Gilbert, D.L., Ridel, K.R., Sallee, F.R., Zhang, J., Lipps, T.D., Wassermann, E.M., Comparison of the inhibitory and excitatory effects of ADHD medications methylphenidate and atomoxetine on motor cortex. Neuropsychopharmacol.: Off. Publ. Am. Coll. Neuropsychopharmacol. 31:2 (2006), 442–449.
21. Glahn, D.C., Ragland, J.D., Abramoff, A., Barrett, J., Laird, A.R., Bearden, C.E., et al. Beyond hypofrontality: a quantitative meta-analysis of functional neuroimaging studies of working memory in schizophrenia. Hum. Brain Map. 25:1 (2005), 60–69.
22. Goldman-Rakic, P.S., Cellular basis of working memory. Neuron 14:3 (1995), 477–485.
23. Grundey, J., Amu, R., Ambrus, G.G., Batsikadze, G., Paulus, W., Nitsche, M.A., Double dissociation of working memory and attentional processes in smokers and non-smokers with and without nicotine. Psychopharmacology 232:14 (2015), 2491–2501.
24. Hart, H., Radua, J., Nakao, T., Mataix-Cols, D., Rubia, K., Meta-analysis of functional magnetic resonance imaging studies of inhibition and attention in attention-deficit/hyperactivity disorder: exploring task-specific, stimulant medication, and age effects. JAMA Psychiatry 70:2 (2013), 185–198.
25. Hester, R., Nandam, L.S., O׳Connell, R.G., Wagner, J., Strudwick, M., Nathan, P.J., et al. Neurochemical enhancement of conscious error awareness. J. Neurosci. 32:8 (2012), 2619–2627.
26. Kimberg, D.Y., D׳Esposito, M., Farah, M.J., Effects of bromocriptine on human subjects depend on working memory capacity. Neuroreport 8:16 (1997), 3581–3585.
27. Lissek, S., Glaubitz, B., Gunturkun, O., Tegenthoff, M., Noradrenergic stimulation modulates activation of extinction-related brain regions and enhances contextual extinction learning without affecting renewal. Front. Behav. Neurosci., 9, 2015, 34.
28. Logemann, H.N., Bocker, K.B., Deschamps, P.K., Kemner, C., Kenemans, J.L., The effect of noradrenergic attenuation by clonidine on inhibition in the stop signal task. Pharmacol., Biochem., Behav. 110 (2013), 104–111.
29. Loughead, J., Wileyto, E.P., Valdez, J.N., Sanborn, P., Tang, K., Strasser, A.A., et al. Effect of abstinence challenge on brain function and cognition in smokers differs by COMT genotype. Mol. Psychiatry 14:8 (2009), 820–826.
30. Marquand, A.F., De Simoni, S., O׳Daly, O.G., Williams, S.C., Mourao-Miranda, J., Mehta, M.A., Pattern classification of working memory networks reveals differential effects of methylphenidate, atomoxetine, and placebo in healthy volunteers. Neuropsychopharmacol.: Off. Publ. Am. Coll. Neuropsychopharmacol. 36:6 (2011), 1237–1247.
31. Marquand, A.F., O׳Daly, O.G., De Simoni, S., Alsop, D.C., Maguire, R.P., Williams, S.C., et al. Dissociable effects of methylphenidate, atomoxetine and placebo on regional cerebral blood flow in healthy volunteers at rest: a multi-class pattern recognition approach. NeuroImage 60:2 (2012), 1015–1024.
32. Mattay, V.S., Goldberg, T.E., Fera, F., Hariri, A.R., Tessitore, A., Egan, M.F., et al. Catechol O-methyltransferase val158-met genotype and individual variation in the brain response to amphetamine. Proc. Natl. Acad. Sci. U. S. A. 100:10 (2003), 6186–6191.
33. McKiernan, K.A., Kaufman, J.N., Kucera-Thompson, J., Binder, J.R., A parametric manipulation of factors affecting task-induced deactivation in functional neuroimaging. J. Cogn. Neurosci. 15:3 (2003), 394–408.
34. McLaren, D.G., Ries, M.L., Xu, G., Johnson, S.C., A generalized form of context-dependent psychophysiological interactions (gPPI): a comparison to standard approaches. NeuroImage 61:4 (2012), 1277–1286.
35. Mehta, M.A., Goodyer, I.M., Sahakian, B.J., Methylphenidate improves working memory and set-shifting in AD/HD: relationships to baseline memory capacity. J. Child Psychol. Psychiatry, Allied Discip. 45:2 (2004), 293–305.
36. Mehta, M.A., Owen, A.M., Sahakian, B.J., Mavaddat, N., Pickard, J.D., Robbins, T.W., Methylphenidate enhances working memory by modulating discrete frontal and parietal lobe regions in the human brain. J. Neurosci., 20(6), 2000, RC65.
37. Menon, V., Uddin, L.Q., Saliency, switching, attention and control: a network model of insula function. Brain Struct. Funct. 214:5-6 (2010), 655–667.
38. Moppett, I.K., Sherman, R.W., Wild, M.J., Latter, J.A., Mahajan, R.P., Effects of norepinephrine and glyceryl trinitrate on cerebral haemodynamics: transcranial Doppler study in healthy volunteers. Br. J. Anaesth. 100:2 (2008), 240–244.
39. Nandam, L.S., Hester, R., Bellgrove, M.A., Dissociable and common effects of methylphenidate, atomoxetine and citalopram on response inhibition neural networks. Neuropsychologia 56 (2014), 263–270.
40. Nandam, L.S., Hester, R., Wagner, J., Cummins, T.D., Garner, K., Dean, A.J., et al. Methylphenidate but not atomoxetine or citalopram modulates inhibitory control and response time variability. Biol. Psychiatry 69:9 (2011), 902–904.
41. Nickel, J., Seitz, R.J., Functional clusters in the human parietal cortex as revealed by an observer-independent meta-analysis of functional activation studies. Anat. Embryol. 210:5-6 (2005), 463–472.
42. Niendam, T.A., Laird, A.R., Ray, K.L., Dean, Y.M., Glahn, D.C., Carter, C.S., Meta-analytic evidence for a superordinate cognitive control network subserving diverse executive functions. Cogn., Affect. Behav. Neurosci. 12:2 (2012), 241–268.
43. O׳Gorman, R.L., Mehta, M.A., Asherson, P., Zelaya, F.O., Brookes, K.J., Toone, B.K., et al. Increased cerebral perfusion in adult attention deficit hyperactivity disorder is normalised by stimulant treatment: a non-invasive MRI pilot study. NeuroImage 42:1 (2008), 36–41.
44. O׳Reilly, J.X., Woolrich, M.W., Behrens, T.E., Smith, S.M., Johansen-Berg, H., Tools of the trade: psychophysiological interactions and functional connectivity. Social. Cogn. Affect. Neurosci. 7:5 (2012), 604–609.
45. Owen, A.M., McMillan, K.M., Laird, A.R., Bullmore, E., N-back working memory paradigm: a meta-analysis of normative functional neuroimaging studies. Hum. Brain Map. 25:1 (2005), 46–59.
46. Power, J.D., Barnes, K.A., Snyder, A.Z., Schlaggar, B.L., Petersen, S.E., Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. NeuroImage 59:3 (2012), 2142–2154.
47. Raabe, M., Fischer, V., Bernhardt, D., Greenlee, M.W., Neural correlates of spatial working memory load in a delayed match-to-sample saccade task. NeuroImage 71 (2013), 84–91.
48. Rae, C.L., Nombela, C., Rodriguez, P.V., Ye, Z., Hughes, L.E., Jones, P.S., et al. Atomoxetine restores the response inhibition network in Parkinson׳s disease. Brain 139:Pt 8 (2016), 2235–2248.
49. Rieckmann, A., Karlsson, S., Fischer, H., Backman, L., Increased bilateral frontal connectivity during working memory in young adults under the influence of a dopamine D1 receptor antagonist. J. Neurosci. 32:48 (2012), 17067–17072.
50. Rowe, J.B., Passingham, R.E., Working memory for location and time: activity in prefrontal area 46 relates to selection rather than maintenance in memory. NeuroImage 14:1 Pt 1 (2001), 77–86.
51. Rowe, J.B., Toni, I., Josephs, O., Frackowiak, R.S., Passingham, R.E., The prefrontal cortex: response selection or maintenance within working memory?. Science 288:5471 (2000), 1656–1660.
52. Saville, C.W., Lancaster, T.M., Stefanou, M.E., Salunkhe, G., Lourmpa, I., Nadkarni, A., et al. COMT Val158Met genotype is associated with fluctuations in working memory performance: converging evidence from behavioural and single-trial P3b measures. NeuroImage 100 (2014), 489–497.
53. Sawaguchi, T., Goldman-Rakic, P.S., 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. 71:2 (1994), 515–528.
54. Seamans, J.K., Gorelova, N., Durstewitz, D., Yang, C.R., Bidirectional dopamine modulation of GABAergic inhibition in prefrontal cortical pyramidal neurons. J. Neurosci. 21:10 (2001), 3628–3638.
55. Sridharan, D., Levitin, D.J., Menon, V., A critical role for the right fronto-insular cortex in switching between central-executive and default-mode networks. Proc. Natl. Acad. Sci. U. S. A. 105:34 (2008), 12569–12574.
56. van den Brink, R.L., Pfeffer, T., Warren, C.M., Murphy, P.R., Tona, K.D., van der Wee, N.J., et al. Catecholaminergic neuromodulation shapes intrinsic MRI functional connectivity in the human brain. J. Neurosci. 36:30 (2016), 7865–7876.
57. Van Snellenberg, J.X., Slifstein, M., Read, C., Weber, J., Thompson, J.L., Wager, T.D., et al. Dynamic shifts in brain network activation during supracapacity working memory task performance. Hum. Brain Map. 36:4 (2015), 1245–1264.
58. Vijayraghavan, S., Wang, M., Birnbaum, S.G., Williams, G.V., Arnsten, A.F., Inverted-U dopamine D1 receptor actions on prefrontal neurons engaged in working memory. Nat. Neurosci. 10:3 (2007), 376–384.
59. Wang, M., Ramos, B.P., Paspalas, C.D., Shu, Y., Simen, A., Duque, A., et al. Alpha2A-adrenoceptors strengthen working memory networks by inhibiting cAMP-HCN channel signaling in prefrontal cortex. Cell 129:2 (2007), 397–410.
60. Wardle, M.C., Hart, A.B., Palmer, A.A., de Wit, H., Does COMT genotype influence the effects of d-amphetamine on executive functioning?. Genes Brain Behav. 12:1 (2013), 13–20.
61. Wechsler, D., Wechsler Adult Intelligence Scale, Fourth Edition, 2008, Pearson, San Antonio, TX, USA.
62. Winterer, G., Musso, F., Vucurevic, G., Stoeter, P., Konrad, A., Seker, B., et al. COMT genotype predicts BOLD signal and noise characteristics in prefrontal circuits. NeuroImage 32:4 (2006), 1722–1732.
63. Witcher, J.W., Long, A., Smith, B., Sauer, J.M., Heilgenstein, J., Wilens, T., et al. Atomoxetine pharmacokinetics in children and adolescents with attention deficit hyperactivity disorder. J. Child Adolesc. Psychopharmacol. 13:1 (2003), 53–63.
64. Ye, Z., Altena, E., Nombela, C., Housden, C.R., Maxwell, H., Rittman, T., et al. Improving response inhibition in Parkinson׳s disease with atomoxetine. Biol. Psychiatry 77:8 (2015), 740–748.
65. Zhang, R., Picchioni, M., Allen, P., Toulopoulou, T., Working memory in unaffected relatives of patients with schizophrenia: a meta-analysis of functional magnetic resonance imaging studies. Schizophr. Bull. 42:4 (2016), 1068–1077.