Methylphenidate modulates interactions of anxiety with cognition.
Journal
Translational psychiatry
ISSN: 2158-3188
Titre abrégé: Transl Psychiatry
Pays: United States
ID NLM: 101562664
Informations de publication
Date de publication:
21 10 2021
21 10 2021
Historique:
received:
08
06
2021
accepted:
13
09
2021
revised:
31
08
2021
entrez:
22
10
2021
pubmed:
23
10
2021
medline:
26
10
2021
Statut:
epublish
Résumé
While a large body of literature documents the impairing effect of anxiety on cognition, performing a demanding task was shown to be effective in reducing anxiety. Here we explored the mechanisms of this anxiolytic effect by examining how a pharmacological challenge designed to improve attentional processes influences the interplay between the neural networks engaged during anxiety and cognition. Using a double-blind between-subject design, we pharmacologically manipulated working memory (WM) using a single oral dose of 20 mg methylphenidate (MPH, cognitive enhancer) or placebo. Fifty healthy adults (25/drug group) performed two runs of a WM N-back task in a 3 T magnetic resonance imaging scanner. This task comprised a low (1-Back) and high (3-Back) WM load, which were performed in two contexts, safety or threat of shocks (induced-anxiety). Analyses revealed that (1) WM accuracy was overall improved by MPH and (2) MPH (vs. placebo) strengthened the engagement of regions within the fronto-parietal control network (FPCN) and reduced the default mode network (DMN) deactivation. These MPH effects predominated in the most difficult context, i.e., threat condition, first run (novelty of the task), and 3-Back task. The facilitation of neural activation can be interpreted as an expansion of cognitive resources, which could foster both the representation and integration of anxiety-provoking stimuli as well as the top-down regulatory processes to protect against the detrimental effect of anxiety. This mechanism might establish an optimal balance between FPCN (cognitive processing) and DMN (emotion regulation) recruitment.
Identifiants
pubmed: 34675189
doi: 10.1038/s41398-021-01621-2
pii: 10.1038/s41398-021-01621-2
pmc: PMC8531440
doi:
Substances chimiques
Methylphenidate
207ZZ9QZ49
Banques de données
ClinicalTrials.gov
['NCT02153944']
Types de publication
Journal Article
Randomized Controlled Trial
Research Support, N.I.H., Intramural
Langues
eng
Sous-ensembles de citation
IM
Pagination
544Subventions
Organisme : Intramural NIH HHS
ID : ZIA MH002798
Pays : United States
Informations de copyright
© 2021. This is a U.S. government work and not under copyright protection in the U.S.; foreign copyright protection may apply.
Références
Airaksinen E, Larsson M, Forsell Y. Neuropsychological functions in anxiety disorders in population-based samples: evidence of episodic memory dysfunction. J Psychiatr Res. 2005;39:207–14.
pubmed: 15589570
doi: 10.1016/j.jpsychires.2004.06.001
Moran TP. Anxiety and working memory capacity: a meta-analysis and narrative review. Psychol Bull. 2016;142:831–64.
pubmed: 26963369
doi: 10.1037/bul0000051
Robinson O, Vytal K, Cornwell BR, Grillon C. The impact of anxiety upon cognition: perspectives from human threat of shock studies. Front Hum Neurosci. 2013;7:203.
pubmed: 23730279
pmcid: 3656338
doi: 10.3389/fnhum.2013.00203
Eysenck MW, Derakshan N. New perspectives in attentional control theory. Pers Individ Differences. 2011;50:955–60.
doi: 10.1016/j.paid.2010.08.019
Balderston NL, Quispe-Escudero D, Hale E, Davis A, O'Connell K, Ernst M, et al. Working memory maintenance is sufficient to reduce state anxiety. Psychophysiology. 2016;53:1660–8.
pubmed: 27434207
pmcid: 5061597
doi: 10.1111/psyp.12726
Clarke R, Johnstone T. Prefrontal inhibition of threat processing reduces working memory interference. Front Hum Neurosci. 2013;7:228.
pubmed: 23750133
pmcid: 3667546
doi: 10.3389/fnhum.2013.00228
Patel N, Vytal K, Pavletic N, Stoodley C, Pine DS, Grillon C, et al. Interaction of threat and verbal working memory in adolescents. Psychophysiology. 2016;53:518–26.
pubmed: 26589772
doi: 10.1111/psyp.12582
Vytal K, Cornwell B, Arkin N, Grillon C. Describing the interplay between anxiety and cognition: from impaired performance under low cognitive load to reduced anxiety under high load. Psychophysiology. 2012;49:842–52.
pubmed: 22332819
pmcid: 3345059
doi: 10.1111/j.1469-8986.2012.01358.x
Vytal KE, Cornwell BR, Letkiewicz AM, Arkin NE, Grillon C. The complex interaction between anxiety and cognition: insight from spatial and verbal working memory. Front Hum Neurosci. 2013;7:93.
pubmed: 23542914
pmcid: 3610083
doi: 10.3389/fnhum.2013.00093
Vytal KE, Arkin NE, Overstreet C, Lieberman L, Grillon C. Induced-anxiety differentially disrupts working memory in generalized anxiety disorder. BMC Psychiatry. 2016;16:1–9.
doi: 10.1186/s12888-016-0748-2
Bishop SJ. Neurocognitive mechanisms of anxiety: an integrative account. Trends Cogn Sci. 2007;11:307–16.
pubmed: 17553730
doi: 10.1016/j.tics.2007.05.008
Eysenck MW, Calvo MG. Anxiety and performance: the processing efficiency theory. Cogn Emot. 1992;6:409–34.
doi: 10.1080/02699939208409696
Eysenck MW, Derakshan N, Santos R, Calvo MG. Anxiety and cognitive performance: attentional control theory. Emotion. 2007;7:336–53.
pubmed: 17516812
doi: 10.1037/1528-3542.7.2.336
Baddeley AD. Working memory. Science. 1992;255:556–9.
doi: 10.1126/science.1736359
Baddeley AD. Is working memory still working?. Am Psychol. 2001;56:851–64.
pubmed: 11785152
doi: 10.1037/0003-066X.56.11.851
Ernst M, Lago T, Davis A, Grillon C. The effects of methylphenidate and propranolol on the interplay between induced-anxiety and working memory. Psychopharmacology. 2016;233:3565–74.
pubmed: 27492789
pmcid: 5131568
doi: 10.1007/s00213-016-4390-y
Fox MD, Raichle ME. Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat Rev Neurosci. 2007;8:700–11.
pubmed: 17704812
doi: 10.1038/nrn2201
Coutinho JF, Fernandesl SV, Soares JM, Maia L, Gonçalves ÓF, Sampaio A. Default mode network dissociation in depressive and anxiety states. Brain Imaging Behav. 2016;10:147–57.
pubmed: 25804311
doi: 10.1007/s11682-015-9375-7
Xiong H, Guo R-J, Shi H-W. Altered default mode network and salience network functional connectivity in patients with generalized anxiety disorders: an ICA-based resting-state fMRI study. Evid Based Complement Alternat Med. 2020;2020:4048916.
pubmed: 32855650
pmcid: 7443230
doi: 10.1155/2020/4048916
Xu J, Van Dam NT, Feng C, Luo Y, Ai H, Gu R, et al. Anxious brain networks: A coordinate-based activation likelihood estimation meta-analysis of resting-state functional connectivity studies in anxiety. Neurosci Biobehav Rev. 2019;96:21–30.
pubmed: 30452934
doi: 10.1016/j.neubiorev.2018.11.005
Sylvester CM, Corbetta M, Raichle ME, Rodebaugh TL, Schlaggar BL, Sheline YI, et al. Functional network dysfunction in anxiety and anxiety disorders. Trends Neurosci. 2012;35:527–35.
pubmed: 22658924
pmcid: 3432139
doi: 10.1016/j.tins.2012.04.012
Mehta MA, Owen AM, Sahakian BJ, Mavaddat N, Pickard JD, Robbins TW. Methylphenidate enhances working memory by modulating discrete frontal and parietal lobe regions in the human brain. J Neurosci. 2000;20:Rc65.
pubmed: 10704519
pmcid: 6772505
doi: 10.1523/JNEUROSCI.20-06-j0004.2000
Volkow ND, Fowler JS, Wang GJ, Telang F, Logan J, Wong C, et al. Methylphenidate decreased the amount of glucose needed by the brain to perform a cognitive task. PLoS ONE. 2008;3:e2017.
pubmed: 18414677
pmcid: 2291196
doi: 10.1371/journal.pone.0002017
Müller U, Suckling J, Zelaya F, Honey G, Faessel H, Williams SC, et al. Plasma level-dependent effects of methylphenidate on task-related functional magnetic resonance imaging signal changes. Psychopharmacology. 2005;180:624–33.
pubmed: 15830222
doi: 10.1007/s00213-005-2264-9
Elliott R, Sahakian BJ, Matthews K, Bannerjea A, Rimmer J, Robbins TW. Effects of methylphenidate on spatial working memory and planning in healthy young adults. Psychopharmacology. 1997;131:196–206.
pubmed: 9201809
doi: 10.1007/s002130050284
First MB. The DSM series and experience with DSM-IV. Psychopathology. 2002;35:67–71.
pubmed: 12145486
doi: 10.1159/000065121
Wechsler D. Manual for the Wechsler abbreviated intelligence scale (WASI). San Antonio, TX: The Psychological Corporation; 1999.
Pauls AM, O'Daly OG, Rubia K, Riedel WJ, Williams SC, Mehta MA. Methylphenidate effects on prefrontal functioning during attentional-capture and response inhibition. Biol Psychiatry. 2012;72:142–9.
pubmed: 22552046
doi: 10.1016/j.biopsych.2012.03.028
Moeller SJ, Honorio J, Tomasi D, Parvaz MA, Woicik PA, Volkow ND, et al. Methylphenidate enhances executive function and optimizes prefrontal function in both health and cocaine addiction. Cereb Cortex. 2014;24:643–53.
pubmed: 23162047
doi: 10.1093/cercor/bhs345
Gualtieri CT, Wargin W, Kanoy R, Patrick K, Shen CD, Youngblood W, et al. Clinical studies of methylphenidate serum levels in children and adults. J Am Acad Child Psychiatry. 1982;21:19–26.
pubmed: 7096827
doi: 10.1097/00004583-198201000-00005
Wargin W, Patrick K, Kilts C, Gualtieri CT, Ellington K, Mueller RA, et al. Pharmacokinetics of methylphenidate in man, rat and monkey. J Pharmacol Exp Therapeutics. 1983;226:382–6.
Nandam LS, Hester R, Bellgrove MA. Dissociable and common effects of methylphenidate, atomoxetine and citalopram on response inhibition neural networks. Neuropsychologia. 2014;56:263–70.
pubmed: 24513025
doi: 10.1016/j.neuropsychologia.2014.01.023
Balderston NL, Vytal KE, O'Connell K, Torrisi S, Letkiewicz A, Ernst M, et al. Anxiety patients show reduced working memory related dlPFC activation during safety and threat. Depress Anxiety. 2017;34:25–36.
pubmed: 27110997
doi: 10.1002/da.22518
Braver TS, Cohen JD, Nystrom LE, Jonides J, Smith EE, Noll DC. A parametric study of prefrontal cortex involvement in human working memory. Neuroimage. 1997;5:49–62.
pubmed: 9038284
doi: 10.1006/nimg.1996.0247
Spielberger CD, Gorsuch RL, Lushene RE, Vagg PR, Jacobs GA. Manual for the state-trait anxiety inventory. Palo Alto, CA: Consulting Psychologists Press; 1983.
Cox RW. AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Computers Biomed Res. 1996;29:162–73.
doi: 10.1006/cbmr.1996.0014
Morey RA, Petty CM, Xu Y, Hayes JP, Wagner HR, Lewis DV, et al. A comparison of automated segmentation and manual tracing for quantifying hippocampal and amygdala volumes. Neuroimage. 2009;45:855–66.
pubmed: 19162198
doi: 10.1016/j.neuroimage.2008.12.033
Fonov V, Evans A, McKinstry R, Almli C, Collins D. Unbiased nonlinear average age-appropriate brain templates from birth to adulthood. Neuroimage. 2009;47:S102.
doi: 10.1016/S1053-8119(09)70884-5
Fonov V, Evans AC, Botteron K, Almli CR, McKinstry RC, Collins DL, et al. Unbiased average age-appropriate atlases for pediatric studies. Neuroimage. 2011;54:313–27.
doi: 10.1016/j.neuroimage.2010.07.033
Collins DL, Zijdenbos AP, Baaré WFC, Evans AC. ANIMAL+INSECT: improved cortical structure segmentation. In: Kuba A, Šáamal M, Todd-Pokropek A, editors. Biennial international conference on information processing in medical imaging. Berlin: Springer; 1999. p. 210–23.
Cox RW, Chen G, Glen DR, Reynolds RC, Taylor PA. FMRI clustering in AFNI: false-positive rates redux. Brain Connectivity. 2017;7:152–71.
pubmed: 28398812
pmcid: 5399747
doi: 10.1089/brain.2016.0475
Bates D, Mächler M, Bolker B, Walker S. Fitting linear mixed-effects models using lme4. J Statistical Software. 2015;67:1–48. Accessed on October 16, 2021 from: https://www.jstatsoft.org/index.php/jss/article/view/v067i01 .
Rapee RM. The utilisation of working memory by worry. Behav Res Ther. 1993;31:617–20.
pubmed: 8347121
doi: 10.1016/0005-7967(93)90114-A
Stout DM, Bomyea J, Risbrough VB, Simmons AN. Aversive distractors modulate affective working memory in frontoparietal regions. Emotion. 2020;20:286–95.
pubmed: 30570314
doi: 10.1037/emo0000544
Linden DEJ. The working memory networks of the human brain. Neuroscientist. 2007;13:257–67.
pubmed: 17519368
doi: 10.1177/1073858406298480
Owen AM, McMillan KM, Laird AR, Bullmore E. N‐back working memory paradigm: a meta‐analysis of normative functional neuroimaging studies. Hum Brain Mapp. 2005;25:46–59.
pubmed: 15846822
pmcid: 6871745
doi: 10.1002/hbm.20131
Nee DE, Brown JW, Askren MK, Berman MG, Demiralp E, Krawitz A, et al. A meta-analysis of executive components of working memory. Cereb Cortex. 2013;23:264–82.
pubmed: 22314046
doi: 10.1093/cercor/bhs007
Crittenden BM, Mitchell DJ, Duncan J. Recruitment of the default mode network during a demanding act of executive control. eLife. 2015;4:e06481.
pubmed: 25866927
pmcid: 4427863
doi: 10.7554/eLife.06481
Smith V, Mitchell DJ, Duncan J. Role of the default mode network in cognitive transitions. Cereb Cortex. 2018;28:3685–96.
pubmed: 30060098
pmcid: 6132281
doi: 10.1093/cercor/bhy167
Uddin LQ, Kelly AM, Biswal BB, Castellanos FX, Milham MP. Functional connectivity of default mode network components: correlation, anticorrelation, and causality. Hum Brain Mapp. 2009;30:625–37.
pubmed: 18219617
doi: 10.1002/hbm.20531
Tomasi D, Volkow ND, Wang GJ, Wang R, Telang F, Caparelli EC, et al. Methylphenidate enhances brain activation and deactivation responses to visual attention and working memory tasks in healthy controls. Neuroimage. 2011;54:3101–10.
pubmed: 21029780
doi: 10.1016/j.neuroimage.2010.10.060
Volkow ND, Wang GJ, Fowler JS, Telang F, Maynard L, Logan J, et al. Evidence that methylphenidate enhances the saliency of a mathematical task by increasing dopamine in the human brain. Am J Psychiatry. 2004;161:1173–80.
pubmed: 15229048
doi: 10.1176/appi.ajp.161.7.1173
Frölich J, Banaschewski T, Döpfner M, Görtz-Dorten A. An evaluation of the pharmacokinetics of methylphenidate for the treatment of attention-deficit/hyperactivity disorder. Expert Opin Drug Metab Toxicol. 2014;10:1169–83.
pubmed: 24856438
doi: 10.1517/17425255.2014.922542
Meléndez JC, McCrank E. Anxiety-related reactions associated with magnetic resonance imaging examinations. JAMA. 1993;270:745–7.
pubmed: 8336378
doi: 10.1001/jama.1993.03510060091039
Tessner KD, Walker EF, Hochman K, Hamann S. Cortisol responses of healthy volunteers undergoing magnetic resonance imaging. Hum Brain Mapp. 2006;27:889–95.
pubmed: 16544325
pmcid: 6871496
doi: 10.1002/hbm.20229
van Maanen L, Forstmann BU, Keuken MC, Wagenmakers EJ, Heathcote A. The impact of MRI scanner environment on perceptual decision-making. Behav Res Methods. 2016;48:184–200.
pubmed: 25701105
doi: 10.3758/s13428-015-0563-6