Transcranial stimulation of the dorsolateral prefrontal cortex prevents stress-induced working memory deficits

Journal of Neuroscience

Volumn 36, Issue 4, 2016, Pages 1429-1437

  Bogdanov, Mario ^a   Schwabe, Lars ^a  

^a UNIVERSITY OF HAMBURG   (Germany)

Author keywords

Brain stimulation; Dorsolateral prefrontal cortex; Glucocorticoids; Stress; Working memory

Indexed keywords

HYDROCORTISONE;

ACUTE STRESS; ADULT; AMNESIA; ARTICLE; BECK DEPRESSION INVENTORY; COGNITIVE DEFECT; CONTROLLED STUDY; DEPRESSION; DIASTOLIC BLOOD PRESSURE; DORSOLATERAL PREFRONTAL CORTEX; DOUBLE BLIND PROCEDURE; FEMALE; HUMAN; HUMAN EXPERIMENT; MALE; MULTIDIMENSIONAL MOOD QUESTIONNAIRE; NORMAL HUMAN; POSTTRAUMATIC STRESS DISORDER; PRIORITY JOURNAL; PULSE RATE; SCHIZOPHRENIA; SYSTOLIC BLOOD PRESSURE; TASK PERFORMANCE; TRANSCRANIAL DIRECT CURRENT STIMULATION; WORKING MEMORY; ANALYSIS OF VARIANCE; COMPLICATION; MEMORY DISORDERS; MENTAL STRESS; METABOLISM; NEUROPSYCHOLOGICAL TEST; PHYSIOLOGY; PREFRONTAL CORTEX; PROCEDURES; RANDOMIZED CONTROLLED TRIAL; SALIVA; SHORT TERM MEMORY; TIME FACTOR; YOUNG ADULT;

ADULT; ANALYSIS OF VARIANCE; DOUBLE-BLIND METHOD; FEMALE; HUMANS; HYDROCORTISONE; MALE; MEMORY DISORDERS; MEMORY, SHORT-TERM; NEUROPSYCHOLOGICAL TESTS; PREFRONTAL CORTEX; SALIVA; STRESS, PSYCHOLOGICAL; TIME FACTORS; TRANSCRANIAL DIRECT CURRENT STIMULATION; YOUNG ADULT;

EID: 84956811517     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3687-15.2016     Document Type: Article

References (85)

1. Andreano JM, Cahill L (2009) Sex influences on the neurobiology of learning and memory. Learn Mem 16:248-266. CrossRef Medline
2. Andrews SC, Hoy KE, Enticott PG, Daskalakis ZJ, Fitzgerald PB (2011) Improving working memory: the effect of combining cognitive activity and anodal transcranial direct current stimulation to the left dorsolateral cortex. Brain Stimul 4:84-89. CrossRef Medline
3. Arnsten AF, Goldman-Rakic PS (1985) Alpha 2-adrenergic mechanisms in prefrontal cortex associated with cognitive decline in aged nonhuman primates. Science 230:1273-1276. CrossRef Medline
4. Arnsten AF (2009) Stress signalling pathways that impair prefrontal cortex structure and function. Nat Rev Neurosci 10:410-422. CrossRef Medline
5. Arnsten AF, Li BM (2005) Neurobiology of executive functions: catecholamine influences on prefrontal cortical functions. Biol Psychiatry 57: 1377-1384. CrossRef Medline
6. Axelrod V, Rees G, Lavidor M, Bar M (2015) Increasing propensity to mindwander with transcranial direct current stimulation. Proc Natl Acad Sci U S A 112:3314-3319. CrossRef Medline
7. Baddeley A (2003) Working memory: looking back and looking forward. Nat Rev Neurosci 4:829-839. CrossRef Medline
8. Barbey AK, Koenigs M, Grafman J (2013) Dorsolateral prefrontal contributions to human working memory. Cortex 49:1195-1205. CrossRef Medline
9. Barsegyan A, Mackenzie SM, Kurose BD, McGaugh JL, Roozendaal B (2010) Glucocorticoids in the prefrontal cortex enhance memory consolidation and impair working memory by a common neural mechanism. Proc Natl Acad Sci U S A 107:16655-16660. CrossRef Medline
10. Baumgartner T, Knoch D, Hotz P, Eisenegger C, Fehr E (2011) Dorsolateral and ventromedial prefrontal cortex orchestrate normative choice. Nat Neurosci 14:1468-1474. CrossRef Medline
11. Beck AT, Steer RA, Brown GK (1996) Manual for the beck depression inventory, Vol 2. San Antonio, TX: Psychological Corporation.
12. Boggio PS, Ferrucci R, Rigonatti SP, Covre P, Nitsche M, Pascual-Leone A, Fregni F (2006) Effects of transcranial direct current stimulation on working memory in patients with Parkinson’s disease. J Neurol Sci 249: 31-38. CrossRef Medline
13. Brozoski TJ, Brown RM, Rosvold HE, Goldman PS (1979) Cognitive deficit caused by regional depletion of dopamine in prefrontal cortex of rhesus monkey. Science 205:929-932. CrossRef Medline
14. Brunoni AR, Nitsche MA, Bolognini N, Bikson M, Wagner T, Merabet L, Edwards DJ, Valero-Cabre A, Rotenberg A, Pascual-Leone A, Ferrucci R, Priori A, Boggio PS, Fregni F (2012) Clinical research with transcranial direct current stimulation (tDCS): challenges and future directions. Brain Stimul 5:175-195. CrossRef Medline
15. Busch RM, Farrell K, Lisdahl-Medina K, Krikorian R (2005) Corsi blocktapping task performance as a function of path configuration. J Clin Exp Neuropsychol 27:127-134. CrossRef Medline
16. Cahill L (2006) Why sex matters for neuroscience. Nat Rev Neurosci 7: 477-484. CrossRef Medline
17. Castaneda AE, Tuulio-Henriksson A, Marttunen M, Suvisaari J, Lonnqvist J (2008) A review on cognitive impairments in depressive and anxiety disorders with a focus on young adults. J Affect Disord 106:1-27. CrossRef Medline
18. Conrad CD, Galea LA, Kuroda Y, McEwen BS (1996) Chronic stress impairs rat spatial memory on the Y maze, and this effect is blocked by tianeptine treatment. Behav Neurosci 110:1321-1334. CrossRef Medline
19. de Kloet ER, Joëls M, Holsboer F (2005) Stress and the brain: from adaptation to disease. Nat Rev Neurosci 6:463-475. CrossRef Medline
20. D’Esposito M, Detre JA, Alsop DC, Shin RK, Atlas S, Grossman M (1995) The neural basis of the central executive system of working memory. Nature 378:279-281. CrossRef Medline
21. D’Esposito M, Aguirre GK, Zarahn E, Ballard D, Shin RK, Lease J (1998) Functional MRI studies of spatial and nonspatial working memory. Brain Res Cogn Brain Res 7:1-13. CrossRef Medline
22. Diamond DM, Park CR, Heman KL, Rose GM (1999) Exposing rats to a predator impairs spatial working memory in the radial arm water maze. Hippocampus 9:542-552. CrossRef Medline
23. Diamond DM, Campbell AM, Park CR, Halonen J, Zoladz PR (2007) The temporal dynamics model of emotional memory processing: a synthesis on the neurobiological basis of stress-induced amnesia, flashbulb and traumatic memories, and the Yerkes-Dodson law. Neural Plast 2007: 1-33. CrossRef Medline
24. Dickerson SS, Kemeny ME (2004) Acute stressors and cortisol responses: a theoretical integration and synthesis of laboratory research. Psychol Bull 130:355-391. CrossRef Medline
25. Eid M, Notz P, Steyer R, Schwenkmezger P (1994) Validating scales for the assessment of mood level and variability by latent state-trait analyses. Pers Individ Dif 16:63-76. CrossRef
26. Elzinga BM, Roelofs K (2005) Cortisol-induced impairments of working memory require acute sympathetic activation. Behav Neurosci 119: 98-103. CrossRef Medline
27. Ferrucci R, Mameli F, Guidi I, Mrakic-Sposta S, Vergari M, Marceglia S, Cogiamanian F, Barbieri S, Scarpini E, Priori A (2008) Transcranial di-rect current stimulation improves recognition memory in Alzheimer disease. Neurology 71:493-498. CrossRef Medline
28. Fox MD, Snyder AZ, Vincent JL, Corbetta M, Van Essen DC, Raichle ME (2005) The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc Natl Acad Sci U S A 102:9673-9678. CrossRef Medline
29. Fregni F, Pascual-Leone A (2007) Technology insight: noninvasive brain stimulation in neurology—perspectives on the therapeutic potential of rTMS and tDCS. Nat Clin Pract Neurol 3:383-393. CrossRef Medline
30. Fregni F, Boggio PS, Nitsche M, Bermpohl F, Antal A, Feredoes E, Marcolin MA, Rigonatti SP, Silva MT, Paulus W, Pascual-Leone A (2005) Anodal transcranial direct current stimulation of prefrontal cortex enhances working memory. Exp Brain Res 166:23-30. CrossRef Medline
31. Fuster JM (1997) Network memory. Trends Neurosci 20:451-459. CrossRef Medline
32. Fuster JM, Alexander GE (1971) Neuron activity related to short-term memory. Science 173:652-654. CrossRef Medline
33. Gerlach KD, Spreng RN, Gilmore AW, Schacter DL (2011) Solving future problems: default network and executive activity associated with goaldirected mental simulations. Neuroimage 55:1816-1824. CrossRef Medline
34. Goldman-Rakic PS (1987) Circuitry of primate prefrontal cortex and regulation of behavior by representational memory. Compr Physiol 373-417.
35. Goldman-Rakic PS (1994) Working memory dysfunction in schizophrenia. J Neuropsychiatry Clin Neurosci 6:348-357. CrossRef Medline
36. Guenzel FM, Wolf OT, Schwabe L (2014) Sex differences in stress effects on response and spatial memory formation. Neurobiol Learn Mem 109: 46-55. CrossRef Medline
37. Haller A, Schwabe L (2014) Sunk costs in the human brain. Neuroimage 97:127-133. CrossRef Medline
38. Harty S, Robertson IH, Miniussi C, Sheehy OC, Devine CA, McCreery S, O’Connell RG (2014) Transcranial direct current stimulation over right dorsolateral prefrontal cortex enhances error awareness in older age. J Neurosci 34:3646-3652. CrossRef Medline
39. Harvey PO, Le Bastard G, Pochon JB, Levy R, Allilaire JF, Dubois B, Fossati P (2004) Executive functions and updating of the contents of working memory in unipolar depression. J Psychiatr Res 38:567-576. CrossRef Medline
40. Honzel N, Justus T, Swick D (2014) Posttraumatic stress disorder is associated with limited executive resources in a working memory task. Cogn Affect Behav Neurosci 14:792-804. CrossRef Medline
41. Hoy KE, Emonson MR, Arnold SL, Thomson RH, Daskalakis ZJ, Fitzgerald PB (2013) Testing the limits: investigating the effect of tDCS dose on working memory enhancement in healthy controls. Neuropsychologia 51:1777-1784. CrossRef Medline
42. Jacobson L, Koslowsky M, Lavidor M (2012) tDCS polarity effects in motor and cognitive domains: a meta-analytical review. Exp Brain Res 216:1-10. CrossRef Medline
43. Jonides J, Smith EE, Koeppe RA, Awh E, Minoshima S, Mintun MA (1993) Spatial working-memory in humans as revealed by PET. Nature 363: 623-625. CrossRef Medline
44. Kessels RP, van den Berg E, Ruis C, Brands AM (2008) The backward span of the Corsi Block-Tapping Task and its association with the WAIS-III Digit Span. Assessment 15:426-434. CrossRef Medline
45. Kincses TZ, Antal A, Nitsche MA, Bártfai O, Paulus W (2004) Facilitation of probabilistic classification learning by transcranial direct current stimulation of the prefrontal cortex in the human. Neuropsychologia 42: 113-117. CrossRef Medline
46. Kirschbaum C, Pirke KM, Hellhammer DH (1993) The ‘Trier Social Stress Test’: a tool for investigating psychobiological stress responses in a laboratory setting. Neuropsychobiology 28:76-81. CrossRef Medline
47. Liebetanz D, Nitsche MA, Tergau F, Paulus W (2002) Pharmacological approach to the mechanisms of transcranial DC-stimulation-induced aftereffects of human motor cortex excitability. Brain 125:2238-2247. CrossRef Medline
48. Lupien SJ, Gillin CJ, Hauger RL (1999) Working memory is more sensitive than declarative memory to the acute effects of corticosteroids: a dose-response study in humans. Behav Neurosci 113:420-430. CrossRef Medline
49. Lupien SJ, Maheu F, Tu M, Fiocco A, Schramek TE (2007) The effects of stress and stress hormones on human cognition: implications for the field of brain and cognition. Brain Cogn 65:209-237. CrossRef Medline
50. Lupien SJ, McEwen BS, Gunnar MR, Heim C (2009) Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nat Rev Neurosci 10:434-445. CrossRef Medline
51. Marshall L, Mölle M, Siebner HR, Born J (2005) Bifrontal transcranial direct current stimulation slows reaction time in a working memory task. BMC Neurosci 6:23. CrossRef Medline
52. Martin KP, Wellman CL (2011) NMDA receptor blockade alters stressinduced dendritic remodeling in medial prefrontal cortex. Cereb Cortex 21:2366-2373. CrossRef Medline
53. McCarthy G, Puce A, Constable RT, Krystal JH, Gore JC, Goldman-Rakic P (1996) Activation of human prefrontal cortex during spatial and nonspatial working memory tasks measured by functional MRI. Cereb Cortex 6:600-611. CrossRef Medline
54. McEwen BS, Morrison JH (2013) The brain on stress: vulnerability and plasticity of the prefrontal cortex over the life course. Neuron 79:16-29. CrossRef Medline
55. Miranda PC, Lomarev M, Hallett M (2006) Modeling the current distribution during transcranial direct current stimulation. Clin Neurophysiol 117:1623-1629. CrossRef Medline
56. Murphy BL, Arnsten AF, Jentsch JD, Roth RH (1996) Dopamine and spatial working memory in rats and monkeys: pharmacological reversal of stressinduced impairment. J Neurosci 16:7768-7775. Medline
57. Nee DE, Brown JW, Askren MK, Berman MG, Demiralp E, Krawitz A, Jonides J (2013) A meta-analysis of executive components of working memory. Cereb Cortex 23:264-282. CrossRef Medline
58. Nitsche MA, Paulus W (2000) Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation. J Physiol 527:633-639. CrossRef Medline
59. Nitsche MA, Fricke K, Henschke U, Schlitterlau A, Liebetanz D, Lang N, Henning S, Tergau F, PaulusW (2003) Pharmacological modulation of cortical excitability shifts induced by transcranial direct current stimulation in humans. J Physiol 533:293-301. CrossRef Medline
60. Nitsche MA, Cohen LG, Wassermann EM, Priori A, Lang N, Antal A, Paulus W, Hummel F, Boggio PS, Fregni F, Pascual-Leone A (2008) Transcranial direct current stimulation: state of the art 2008. Brain Stimul 1: 206-223. CrossRef Medline
61. Pessoa L (2008) On the relationship between emotion and cognition. Nat Rev Neurosci 9:148-158. CrossRef Medline
62. Pope PA, Brenton JW, Miall RC (2015) Task-specific facilitation of cognition by anodal transcranial direct current stimulation of the prefrontal cortex. Cereb Cortex 25:4551-4558. CrossRef Medline
63. Prager EM, Johnson LR (2009) Stress at the synapse: signal transduction mechanisms of adrenal steroids at neuronal membranes. Sci Signal 2:re5. CrossRef Medline
64. Qin S, Hermans EJ, van Marle HJ, Luo J, Fernández G (2009) Acute psychological stress reduces working memory-related activity in the dorsolateral prefrontal cortex. Biol Psychiatry 66:25-32. CrossRef Medline
65. Roozendaal B, McReynolds JR, McGaugh JL (2004) The basolateral amygdala interacts with the medial prefrontal cortex in regulating glucocorticoid effects on working memory impairment. J Neurosci 24: 1385-1392. CrossRef Medline
66. Roozendaal B, McEwen BS, Chattarji S (2009) Stress, memory and the amygdala. Nat Rev Neurosci 10:423-433. CrossRef Medline
67. Rottschy C, Langner R, Dogan I, Reetz K, Laird AR, Schulz JB, Fox PT, Eickhoff SB (2012) Modelling neural correlates of working memory: a coordinate-based meta-analysis. Neuroimage 60:830-846. CrossRef Medline
68. Sandi C, Haller J (2015) Stress and the social brain: behavioural effects and neurobiological mechanisms. Nat Rev Neurosci 16:290-304. CrossRef Medline
69. Schoofs D, Wolf OT, Smeets T (2009) Cold pressor stress impairs performance on working memory tasks requiring executive functions in healthy young men. Behav Neurosci 123:1066-1075. CrossRef Medline
70. Schulz P, Schlotz W (1999) The Trier Inventory for the Assessment of Chronic Stress (TICS): scale construction, statistical testing, and validation of the scale work overload. Diagnostica 45:8-19. CrossRef
71. Schwabe L, Wolf OT (2013) Stress and multiple memory systems: from ‘thinking’to ‘doing.’ Trends Cogn Sci 17:60-68. CrossRef Medline
72. Schwabe L, Joëls M, Roozendaal B, Wolf OT, Oitzl MS (2012) Stress effects on memory: an update and integration. Neurosci Biobehav Rev 36: 1740-1749. CrossRef Medline
73. Smeets T, Cornelisse S, Quaedflieg CW, Meyer T, Jelicic M, Merckelbach H (2012) Introducing the Maastricht Acute Stress Test (MAST): a quick and non-invasive approach to elicit robust autonomic and glucocorticoid stress responses. Psychoneuroendocrinology 37:1998-2008. CrossRef Medline
74. Smith EE, Jonides J (1997) Working memory: a view from neuroimaging. Cogn Psychol 33:5-42. CrossRef Medline
75. Snyder HR (2013) Major depressive disorder is associated with broad impairments on neuropsychological measures of executive function: a metaanalysis and review. Psychol Bull 139:81-132. CrossRef Medline
76. Sparing R, Dafotakis M, Meister IG, Thirugnanasambandam N, Fink GR (2008) Enhancing language performance with non-invasive brain stimulation: a transcranial direct current stimulation study in healthy humans. Neuropsychologia 46:261-268. CrossRef Medline
77. Sreenivasan KK, Curtis CE, D’Esposito M (2014) Revisiting the role of persistent neural activity during working memory. Trends Cogn Sci 18: 82-89. CrossRef Medline
78. Stagg CJ, Lin RL, Mezue M, Segerdahl A, Kong Y, Xie J, Tracey I (2013) Widespread modulation of cerebral perfusion induced during and after transcranial direct current stimulation applied to the left dorsolateral prefrontal cortex. J Neurosci 33:11425-11431. CrossRef Medline
79. Tabachnick BG, Fidell LS (2005) Using multivariate statistics. Boston: Allyn and Bacon.
80. Wagner S, Rampersad SM, Aydin Ü, Vorwerk J, Oostendorp TF, Neuling T, Herrmann CS, Stegeman DF, Wolters CH (2014) Investigation of tDCS volume conduction effects in a highly realistic head model. J Neural Eng 11:1-14. CrossRef Medline
81. Weber MJ, Messing SB, Rao H, Detre JA, Thompson-Schill SL (2014) Prefrontal transcranial direct current stimulation alters activation and connectivity in cortical and subcortical reward systems: a tDCS-fMRI study. Hum Brain Mapp 35:3673-3686. CrossRef Medline
82. Wechsler D (1997) Wechsler memory scale (WMS-III). San Antonio: Psychological Corporation.
83. Wechsler D (2008) Wechsler adult intelligence scale, Ed 4 (WAIS-IV). San Antonio: NCS Pearson.
84. Zaehle T, Sandmann P, Thorne JD, Jäncke L, Herrmann CS (2011) Transcranial direct current stimulation of the prefrontal cortex modulates working memory performance: combined behavioural and electrophysiological evidence. BMC Neurosci 12:1-11. CrossRef Medline
85. Zwissler B, Sperber C, Aigeldinger S, Schindler S, Kissler J, Plewnia C (2014) Shaping memory accuracy by left prefrontal transcranial direct current stimulation. J Neurosci 34:4022-4026. CrossRef Medline