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Dorsolateral prefrontal cortex, working memory and episodic memory processes: insight through transcranial magnetic stimulation techniques

Abstract

The ability to recall and recognize facts we experienced in the past is based on a complex mechanism in which several cerebral regions are implicated. Neuroimaging and lesion studies agree in identifying the frontal lobe as a crucial structure for memory processes, and in particular for working memory and episodic memory and their relationships. Furthermore, with the introduction of transcranial magnetic stimulation (TMS) a new way was proposed to investigate the relationships between brain correlates, memory functions and behavior. The aim of this review is to present the main findings that have emerged from experiments which used the TMS technique for memory analysis. They mainly focused on the role of the dorsolateral prefrontal cortex in memory process. Furthermore, we present state-of-the-art evidence supporting a possible use of TMS in the clinic. Specifically we focus on the treatment of memory deficits in depression and anxiety disorders.

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References

  1. [1]

    Moscovitch, A. Neuropsychology of Memory. 2nd ed. New York: Guilford Press, 1992: 5–22.

    Google Scholar 

  2. [2]

    Brenda Milner MP. Behavioural effects of frontal-lobe lesions in man. Trends Neurosci 1984, 7: 403–407.

    Article  Google Scholar 

  3. [3]

    Petrides M. Frontal Lobes and Memory. 2nd ed. New York: Elsevier Science Publishers, 1989: 75–90.

    Google Scholar 

  4. [4]

    Fletcher PC, Shallice T, Frith CD, Frackowiak RS, Dolan RJ. The functional roles of prefrontal cortex in episodic memory. ii. Retrieval. Brain 1998, 121( Pt 7): 1249–1256.

    PubMed  Article  Google Scholar 

  5. [5]

    Curtis CE, D’Esposito M. Persistent activity in the prefrontal cortex during working memory. Trends Cogn Sci 2003, 7: 415–423.

    PubMed  Article  Google Scholar 

  6. [6]

    Tulving E. Précis of Elements of episodic memory. Behav Brain Sci 1984, 7: 223–268.

    Article  Google Scholar 

  7. [7]

    Baddeley A. The episodic buffer: a new component of working memory? Trends Cogn Sci 2000, 4: 417–423.

    PubMed  Article  Google Scholar 

  8. [8]

    Papagno C. Neuropsicologia della Memoria [Neuropsychology of Memory]. Bologna: Il Mulino, 2010.

    Google Scholar 

  9. [9]

    Blumenfeld RS, Ranganath C. Dorsolateral prefrontal cortex promotes long-term memory formation through its role in working memory organization. J Neurosci 2006, 26: 916–925.

    PubMed  Article  CAS  Google Scholar 

  10. [10]

    Sandrini M, Cappa SF, Rossi S, Rossini PM, Miniussi C. The role of prefrontal cortex in verbal episodic memory: rTMS evidence. J Cogn Neurosci 2003, 15: 855–861.

    PubMed  Article  Google Scholar 

  11. [11]

    Schmidt D, Krause BJ, Mottaghy FM, Halsband U, Herzog H, Tellmann L, et al. Brain systems engaged in encoding and retrieval of word-pair associates independent of their imagery content or presentation modalities. Neuropsychologia 2002, 40: 457–470.

    PubMed  Article  CAS  Google Scholar 

  12. [12]

    Johnson MK, Multhaup KS. The Handbook of Emotion and Memory: Current Research and Theory. Hillsdale: Erlbaum Associates, 1992: 33–66.

    Google Scholar 

  13. [13]

    Nolde SF, Johnson MK, Raye CL. The role of prefrontal cortex during tests of episodic memory. Trends Cogn Sci 1998, 2: 399–406.

    PubMed  Article  CAS  Google Scholar 

  14. [14]

    Miniussi C, Ruzzoli M, Walsh V. The mechanism of transcranial magnetic stimulation in cognition. Cortex 2010, 46: 128–130.

    PubMed  Article  Google Scholar 

  15. [15]

    Chen R, Classen J, Gerloff C, Celnik P, Wassermann EM, Hallett M, et al. Depression of motor cortex excitability by low-frequency transcranial magnetic stimulation. Neurology 1997, 48: 1398–1403.

    PubMed  Article  CAS  Google Scholar 

  16. [16]

    George MS, Padberg F, Schlaepfer TE, O’Reardon JP, Fitzgerald PB, Nahas ZH, et al. Controversy: Repetitive transcranial magnetic stimulation or transcranial direct current stimulation shows efficacy in treating psychiatric diseases (depression, mania, schizophrenia, obsessive-complusive disorder, panic, posttraumatic stress disorder). Brain Stimul 2009, 2: 14–21.

    PubMed  Article  Google Scholar 

  17. [17]

    Thut G, Pascual-Leone A. A review of combined TMS-EEG studies to characterize lasting effects of repetitive TMS and assess their usefulness in cognitive and clinical neuroscience. Brain Topogr 2010, 22: 219–232.

    PubMed  Article  Google Scholar 

  18. [18]

    Pascual-Leone A, Hallett M. Induction of errors in a delayed response task by repetitive transcranial magnetic stimulation of the dorsolateral prefrontal cortex. Neuroreport 1994, 5: 2517–2520.

    PubMed  Article  CAS  Google Scholar 

  19. [19]

    Jahanshahi M, Profice P, Brown RG, Ridding MC, Dirnberger G, Rothwell JC. The effects of transcranial magnetic stimulation over the dorsolateral prefrontal cortex on suppression of habitual counting during random number generation. Brain 1998, 121(Pt 8): 1533–1544.

    PubMed  Article  Google Scholar 

  20. [20]

    Mottaghy FM, Krause BJ, Kemna LJ, Topper R, Tellmann L, Beu M, et al. Modulation of the neuronal circuitry subserving working memory in healthy human subjects by repetitive transcranial magnetic stimulation. Neurosci Lett 2000, 280: 167–170.

    PubMed  Article  CAS  Google Scholar 

  21. [21]

    Mottaghy FM, Gangitano M, Krause BJ, Pascual-Leone A. Chronometry of parietal and prefrontal activations in verbal working memory revealed by transcranial magnetic stimulation. Neuroimage 2003, 18: 565–575.

    PubMed  Article  CAS  Google Scholar 

  22. [22]

    Postle BR, Ferrarelli F, Hamidi M, Feredoes E, Massimini M, Peterson M, et al. Repetitive transcranial magnetic stimulation dissociates working memory manipulation from retention functions in the prefrontal, but not posterior parietal, cortex. J Cogn Neurosci 2006, 18: 1712–1722.

    PubMed  Article  Google Scholar 

  23. [23]

    Osaka N, Otsuka Y, Hirose N, Ikeda T, Mima T, Fukuyama H, et al. Transcranial magnetic stimulation (TMS) applied to left dorsolateral prefrontal cortex disrupts verbal working memory performance in humans. Neurosci Lett 2007, 418: 232–235.

    PubMed  Article  CAS  Google Scholar 

  24. [24]

    Preston G, Anderson E, Silva C, Goldberg T, Wassermann EM. Effects of 10 Hz rTMS on the neural efficiency of working memory. J Cogn Neurosci 2010, 22: 447–456.

    PubMed  Article  Google Scholar 

  25. [25]

    Mull BR, Seyal M. Transcranial magnetic stimulation of left prefrontal cortex impairs working memory. Clin Neurophysiol 2001, 112: 1672–1675.

    PubMed  Article  CAS  Google Scholar 

  26. [26]

    Hadland KA, Rushworth MF, Passingham RE, Jahanshahi M, Rothwell JC. Interference with performance of a response selection task that has no working memory component: an rTMS comparison of the dorsolateral prefrontal and medial frontal cortex. J Cogn Neurosci 2001, 13: 1097–1108.

    PubMed  Article  CAS  Google Scholar 

  27. [27]

    Chao LL, Knight RT. Contribution of human prefrontal cortex to delay performance. J Cogn Neurosci 1998, 10: 167–177.

    PubMed  Article  CAS  Google Scholar 

  28. [28]

    Hannula H, Neuvonen T, Savolainen P, Hiltunen J, Ma YY, Antila H, et al. Increasing top-down suppression from prefrontal cortex facilitates tactile working memory. Neuroimage 2010, 49: 1091–1098.

    PubMed  Article  Google Scholar 

  29. [29]

    Gagnon G, Blanchet S, Grondin S, Schneider C. Pairedpulse transcranial magnetic stimulation over the dorsolateral prefrontal cortex interferes with episodic encoding and retrieval for both verbal and non-verbal materials. Brain Res 2010, 1344: 148–158.

    PubMed  Article  CAS  Google Scholar 

  30. [30]

    Gagnon G, Schneider C, Grondin S, Blanchet S. Enhancement of episodic memory in young and healthy adults: a paired-pulse TMS study on encoding and retrieval performance. Neurosci Lett 2011, 488: 138–142.

    PubMed  Article  CAS  Google Scholar 

  31. [31]

    Rossi S, Cappa SF, Babiloni C, Pasqualetti P, Miniussi C, Carducci F, et al. Prefrontal [correction of Prefontal]_cortex in long-term memory: an “interference” approach using magnetic stimulation. Nat Neurosci 2001, 4: 948–952.

    PubMed  Article  CAS  Google Scholar 

  32. [32]

    Innocenti I, Giovannelli F, Cincotta M, Feurra M, Polizzotto NR, Bianco G, et al. Event-related rTMS at encoding affects differently deep and shallow memory traces. Neuroimage 2010, 53: 325–330.

    PubMed  Article  Google Scholar 

  33. [33]

    Manenti R, Tettamanti M, Cotelli M, Miniussi C, Cappa SF. The neural bases of word encoding and retrieval: A fMRI-guided transcranial magnetic stimulation study. Brain Topogr 2010, 22: 318–332.

    PubMed  Article  CAS  Google Scholar 

  34. [34]

    Paivio A. Dual coding theory: Retrospect and current status. Can J Psychol 1991, 45: 255–287.

    Article  Google Scholar 

  35. [35]

    Kishiyama MM, Yonelinas AP, Knight RT. Novelty enhancements in memory are dependent on lateral prefrontal cortex. J Neurosci 2009, 29: 8114–8118.

    PubMed  Article  CAS  Google Scholar 

  36. [36]

    Skrdlantova L, Horacek J, Dockery C, Lukavsky J, Kopecek M, Preiss M, et al. The influence of low-frequency left prefrontal repetitive transcranial magnetic stimulation on memory for words but not for faces. Physiol Res 2005, 54: 123–128.

    PubMed  CAS  Google Scholar 

  37. [37]

    Floel A, Poeppel D, Buffalo EA, Braun A, Wu CW, Seo HJ, et al. Prefrontal cortex asymmetry for memory encoding of words and abstract shapes. Cereb Cortex 2004, 14: 404–409.

    PubMed  Article  Google Scholar 

  38. [38]

    Epstein CM, Sekino M, Yamaguchi K, Kamiya S, Ueno S. Asymmetries of prefrontal cortex in human episodic memory: effects of transcranial magnetic stimulation on learning abstract patterns. Neurosci Lett 2002, 320: 5–8.

    PubMed  Article  CAS  Google Scholar 

  39. [39]

    Balconi M, Ferrari C. Emotional memory retrieval. rTMS stimulation on left DLPFC increases the positive memories. Brain imaging Behav 2012, 6: 454–461.

    PubMed  Article  Google Scholar 

  40. [40]

    Balconi M, Ferrari C. rTMS stimulation on left DLPFC increases the correct recognition of memories for emotional target and distractor words. Cogn Affect Behav Neurosci 2012, 12: 589–598.

    PubMed  Article  Google Scholar 

  41. [41]

    Bishop S, Duncan J, Brett M, Lawrence AD. Prefrontal cortical function and anxiety: controlling attention to threat-related stimuli. Nat Neurosci 2004, 7: 184–188.

    PubMed  Article  CAS  Google Scholar 

  42. [42]

    Tucker DM, Antes JR, Stenslie CE, Barnhardt TM. Anxiety and lateral cerebral function. J Abnorm Psychol 1978, 87: 380–383.

    PubMed  Article  CAS  Google Scholar 

  43. [43]

    Carter WR, Johnson MC, Borkovec TD. Worry: An electrocortical analysis. Adv Behav Res Ther 1986, 4: 193–204.

    Article  Google Scholar 

  44. [44]

    Baxter LR Jr, Schwartz JM, Phelps ME, Mazziotta JC, Guze BH, Selin CE, et al. Reduction of prefrontal cortex glucose metabolism common to three types of depression. Arch Gen Psychiatry 1989, 46: 243–250.

    PubMed  Article  CAS  Google Scholar 

  45. [45]

    Heller W, Etienne MA, Miller GA. Patterns of perceptual asymmetry in depression and anxiety: implications for neuropsychological models of emotion and psychopathology. J Abnorm Psychol 1995, 104: 327–333.

    PubMed  Article  CAS  Google Scholar 

  46. [46]

    Buchsbaum MS, Wu J, Haier R, Hazlett E, Ball R, Katz M, et al. Positron emission tomography assessment of effects of benzodiazepines on regional glucose metabolic rate in patients with anxiety disorder. Life Sci 1987, 40: 2393–2400.

    PubMed  Article  CAS  Google Scholar 

  47. [47]

    Balconi M, Brambilla E, Falbo L. Appetitive vs. defensive responses to emotional cues. Autonomic measures and brain oscillation modulation. Brain Res 2009, 1296: 72–84.

    PubMed  Article  CAS  Google Scholar 

  48. [48]

    Davidson RJ, Irwin W. The functional neuroanatomy of emotion and affective style. Trends Cogn Sci 1999, 3: 11–21.

    PubMed  Article  Google Scholar 

  49. [49]

    Zwanzger P, Fallgatter AJ, Zavorotnyy M, Padberg F. Anxiolytic effects of transcranial magnetic stimulation—an alternative treatment option in anxiety disorders? J Neural Transm 2009, 116: 767–775.

    PubMed  Article  Google Scholar 

  50. [50]

    van Honk J, Tuiten A, Verbaten R, van den Hout M, Koppeschaar H, Thijssen J, et al. Correlations among salivary testosterone, mood, and selective attention to threat in humans. Horm Behav 1999, 36: 17–24.

    PubMed  Article  Google Scholar 

  51. [51]

    Bench CJ, Frackowiak RS, Dolan RJ. Changes in regional cerebral blood flow on recovery from depression. Psychol Med 1995, 25: 247–261.

    PubMed  Article  CAS  Google Scholar 

  52. [52]

    Drevets WC. Functional anatomical abnormalities in limbic and prefrontal cortical structures in major depression. Prog Brain Res 2000, 126: 413–431.

    PubMed  Article  CAS  Google Scholar 

  53. [53]

    Pascual-Leone A, Catala MD, Pascual-Leone Pascual A. Lateralized effect of rapid-rate transcranial magnetic stimulation of the prefrontal cortex on mood. Neurology 1996, 46: 499–502.

    PubMed  Article  CAS  Google Scholar 

  54. [54]

    Gross M, Nakamura L, Pascual-Leone A, Fregni F. Has repetitive transcranial magnetic stimulation (rTMS) treatment for depression improved? A systematic review and metaanalysis comparing the recent vs. the earlier rTMS studies. Acta Psychiatr Scand 2007, 116: 165–173.

    PubMed  Article  CAS  Google Scholar 

  55. [55]

    Martin JL, Barbanoj MJ, Schlaepfer TE, Thompson E, Perez V, Kulisevsky J. Repetitive transcranial magnetic stimulation for the treatment of depression. Systematic review and metaanalysis. Br J Psychiatry 2003, 182: 480–491.

    PubMed  Article  Google Scholar 

  56. [56]

    Weiland-Fiedler P, Erickson K, Waldeck T, Luckenbaugh DA, Pike D, Bonne O, et al. Evidence for continuing neuropsychological impairments in depression. J Affect Disord 2004, 82: 253–258.

    PubMed  Article  Google Scholar 

  57. [57]

    Brand AN, Jolles J, Gispen-de Wied C. Recall and recognition memory deficits in depression. J Affect Disord 1992, 25: 77–86.

    PubMed  Article  CAS  Google Scholar 

  58. [58]

    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: 207–214.

    PubMed  Article  Google Scholar 

  59. [59]

    Sole-Padulles C, Bartres-Faz D, Junque C, Clemente IC, Molinuevo JL, Bargallo N, et al. Repetitive transcranial magnetic stimulation effects on brain function and cognition among elders with memory dysfunction. A randomized shamcontrolled study. Cereb Cortex 2006, 16: 1487–1493.

    PubMed  Article  Google Scholar 

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Correspondence to Michela Balconi.

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Balconi, M. Dorsolateral prefrontal cortex, working memory and episodic memory processes: insight through transcranial magnetic stimulation techniques. Neurosci. Bull. 29, 381–389 (2013). https://doi.org/10.1007/s12264-013-1309-z

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Keywords

  • transcranial magnetic stimulation
  • dorsolateral prefrontal cortex
  • memory
  • working memory
  • anxiety
  • depression