Task-dependent activity and connectivity predict episodic memory network-based responses to brain stimulation in healthy aging

Brain Stimulation

Volumn 7, Issue 2, 2014, Pages 287-296

  Vidal Piñeiro, Dídac ^a   Martin Trias, Pablo ^a   Arenaza Urquijo, Eider M ^a   Sala Llonch, Roser ^a   Clemente, Imma C ^a,b   Mena Sánchez, Isaias ^a   Bargalló, Núria ^c,d   Falcón, Carles ^c,e   Pascual Leone, Álvaro ^f,g   Bartrés Faz, David ^a,c  

^a UNIVERSITY OF BARCELONA   (Spain)

^b Institute for Brain Cognition and Behavior (IR3C)   (Spain)

^c INSTITUT D INVESTIGACIONS BIOMÈDIQUES AUGUST PI I SUNYER IDIBAPS   (Spain)

^d CSU de Bellvitge   (Spain)

^e BIOMATERIALES Y NANOMEDICINA CIBER BBN   (Spain)

^f HARVARD MEDICAL SCHOOL   (United States)

^g University Institute affiliated with the Autonomous University of Barcelona   (Spain)

Author keywords

Aging; Episodic memory; Functional magnetic resonance imaging; Level of processing; Transcranial magnetic stimulation

Indexed keywords

ADULT; AGED; AGING; ARTICLE; BOLD SIGNAL; CEREBELLUM; EPISODIC MEMORY; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HUMAN EXPERIMENT; INFERIOR FRONTAL GYRUS; MALE; MENTAL PERFORMANCE; MIDDLE AGED; NERVE CELL NETWORK; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE SCANNER; OCCIPITAL CORTEX; ORBITAL CORTEX; PRIORITY JOURNAL; STRIATE CORTEX; SUPERIOR FRONTAL GYRUS; SUPPLEMENTARY MOTOR AREA; TRANSCRANIAL MAGNETIC STIMULATION; TRANSCRANIAL MAGNETIC STIMULATION SYSTEM; VERY ELDERLY; BRAIN; BRAIN MAPPING; NEUROPSYCHOLOGICAL TEST; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY; PROCEDURES;

AGED; AGED, 80 AND OVER; AGING; BRAIN; BRAIN MAPPING; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MEMORY, EPISODIC; MIDDLE AGED; NERVE NET; NEUROPSYCHOLOGICAL TESTS; TRANSCRANIAL MAGNETIC STIMULATION;

EID: 84896394981     PISSN: 1935861X     EISSN: 18764754     Source Type: Journal    
DOI: 10.1016/j.brs.2013.12.016     Document Type: Article

References (95)

1. P.A. Reuter-Lorenz, and D.C. Park Human neuroscience and the aging mind: a new look at old problems J Gerontol B Psychol Sci Soc Sci 65 2010 405 415.
2. D.C. Park, and P. Reuter-Lorenz The adaptive brain: aging and neurocognitive scaffolding Annu Rev Psychol 60 2009 173 196.
3. B. Guse, P. Falkai, and T. Wobrock Cognitive effects of high-frequency repetitive transcranial magnetic stimulation: a systematic review J Neural Transm 117 2010 105 122.
4. S. Tanaka, M. Sandrini, and L.G. Cohen Modulation of motor learning and memory formation by non-invasive cortical stimulation of the primary motor cortex Neuropsychol Rehabil 21 2011 650 675.
5. C. Solé-Padullés, D. Bartrés-Faz, C. Junqué, I.C. Clemente, J.L. Molinuevo, and N. Bargalló et al. Repetitive transcranial magnetic stimulation effects on brain function and cognition among elders with memory dysfunction. A randomized sham-controlled study Cereb Cortex 16 2006 1487 1493.
6. R. Ferrucci, F. Mameli, I. Guidi, S. Mrakic-Sposta, M. Vergari, and S. Marceglia et al. Transcranial direct current stimulation improves recognition memory in Alzheimer disease Neurology 71 2008 493 498.
7. M. Cotelli, R. Manenti, S. Rosini, M. Calabria, M. Brambilla, and P.S. Bisiacchi et al. Action and object naming in physiological aging: an rTMS study Front Aging Neurosci 2 2010 151.
8. M. Cotelli, M. Calabria, R. Manenti, S. Rosini, O. Zanetti, and S.F. Cappa et al. Improved language performance in Alzheimer disease following brain stimulation J Neurol Neurosurg Psychiatry 82 2011 794 797.
9. J. O'Shea, H. Johansen-Berg, D. Trief, S. Göbel, and M.F.S. Rushworth Functionally specific reorganization in human premotor cortex Neuron 54 2007 479 490.
10. S. Bestmann, O. Swayne, F. Blankenburg, C.C. Ruff, P. Haggard, and N. Weiskopf et al. Dorsal premotor cortex exerts state-dependent causal influences on activity in contralateral primary motor and dorsal premotor cortex Cereb Cortex 18 2008 1281 1291.
11. J. Silvanto, N. Muggleton, and V. Walsh State-dependency in brain stimulation studies of perception and cognition Trends Cogn Sci 12 2008 447 454.
12. T.G. Lee, and M. D'Esposito The dynamic nature of top-down signals originating from prefrontal cortex: a combined fMRI-TMS study J Neurosci 32 2012 15458 15466.
13. L. Cárdenas-Morales, L.J. Volz, J. Michely, A.K. Rehme, E.-M. Pool, and C. Nettekoven et al. Network connectivity and individual responses to brain stimulation in the human motor system Cereb Cortex 2013.
14. E.R. Buch, V.M. Johnen, N. Nelissen, J. O'Shea, and M.F.S. Rushworth Noninvasive associative plasticity induction in a corticocortical pathway of the human brain J Neurosci 31 2011 17669 17679.
15. C. Freitas, J. Perez, M. Knobel, J.M. Tormos, L. Oberman, and M. Eldaief et al. Changes in cortical plasticity across the lifespan Front Aging Neurosci 3 2011 5.
16. B.J. Cheeran, C. Ritter, J.C. Rothwell, and H.R. Siebner Mapping genetic influences on the corticospinal motor system in humans Neuroscience 164 2009 156 163.
17. T. Wagner, A. Valero-Cabre, and A. Pascual-Leone Noninvasive human brain stimulation Annu Rev Biomed Eng 9 2007 527 565.
18. F.A. Kozel, Z. Nahas, C. deBrux, M. Molloy, J.P. Lorberbaum, and D. Bohning et al. How coil-cortex distance relates to age, motor threshold, and antidepressant response to repetitive transcranial magnetic stimulation J Neuropsychiatry Clin Neurosci 12 2000 376 384.
19. C.J. Stagg, J. O'Shea, and H. Johansen-Berg Imaging the effects of rTMS-induced cortical plasticity Restor Neurol Neurosci 28 2010 425 436.
20. J. Reithler, J.C. Peters, and A.T. Sack Multimodal transcranial magnetic stimulation: using concurrent neuroimaging to reveal the neural network dynamics of noninvasive brain stimulation Prog Neurobiol 94 2011 149 165.
21. Y.-Z. Huang, M.J. Edwards, E. Rounis, K.P. Bhatia, and J.C. Rothwell Theta burst stimulation of the human motor cortex Neuron 45 2005 201 206.
22. H.M. Morgan, M.C. Jackson, M.G. van Koningsbruggen, K.L. Shapiro, and D.E.J. Linden Frontal and parietal theta burst TMS impairs working memory for visual-spatial conjunctions Brain Stimul 6 2013 122 129.
23. J. Restle, T. Murakami, and U. Ziemann Facilitation of speech repetition accuracy by theta burst stimulation of the left posterior inferior frontal gyrus Neuropsychologia 50 2012 2026 2031.
24. I. Volman, K. Roelofs, S. Koch, L. Verhagen, and I. Toni Anterior prefrontal cortex inhibition impairs control over social emotional actions Curr Biol 21 2011 1766 1770.
25. M. Sandrini, S.F. Cappa, S. Rossi, P.M. Rossini, and C. Miniussi The role of prefrontal cortex in verbal episodic memory: rTMS evidence J Cogn Neurosci 15 2003 855 861.
26. S. Rossi, C. Miniussi, P. Pasqualetti, C. Babiloni, P.M. Rossini, and S.F. Cappa Age-related functional changes of prefrontal cortex in long-term memory: a repetitive transcranial magnetic stimulation study J Neurosci 24 2004 7939 7944.
27. I. Innocenti, F. Giovannelli, M. Cincotta, M. Feurra, N.R. Polizzotto, and G. Bianco et al. Event-related rTMS at encoding affects differently deep and shallow memory traces NeuroImage 53 2010 325 330.
28. S. Köhler, T. Paus, R.L. Buckner, and B. Milner Effects of left inferior prefrontal stimulation on episodic memory formation: a two-stage fMRI-rTMS study J Cogn Neurosci 16 2004 178 188.
29. I. Kahn, A. Pascual-Leone, H. Theoret, F. Fregni, D. Clark, and A.D. Wagner Transient disruption of ventrolateral prefrontal cortex during verbal encoding affects subsequent memory performance J Neurophysiol 94 2005 688 698.
30. M.G. Machizawa, R. Kalla, V. Walsh, and L.J. Otten The time course of ventrolateral prefrontal cortex involvement in memory formation J Neurophysiol 103 2010 1569 1579.
31. S. Kapur, F.I. Craik, E. Tulving, A.A. Wilson, S. Houle, and G.M. Brown Neuroanatomical correlates of encoding in episodic memory: levels of processing effect Proc Natl Acad Sci U S A 91 1994 2008 2011.
32. A.D. Wagner, D.L. Schacter, M. Rotte, W. Koutstaal, A. Maril, and A.M. Dale et al. Building memories: remembering and forgetting of verbal experiences as predicted by brain activity Science 281 1998 1188 1191.
33. L.J. Otten, R.N. Henson, and M.D. Rugg Depth of processing effects on neural correlates of memory encoding: relationship between findings from across- and within-task comparisons Brain J Neurol 124 2001 399 412.
34. F.I.M. Craik, and R.S. Lockhart Levels of processing: a framework for memory research J Verbal Learn Verbal Behav 11 1972 671 684.
35. F. Craik, and E. Tulving Depth of processing and the retention of words in episodic memory J Exp Psychol Gen 104 1975 268 294.
36. J.M. Logan, A.L. Sanders, A.Z. Snyder, J.C. Morris, and R.L. Buckner Under-recruitment and nonselective recruitment: dissociable neural mechanisms associated with aging Neuron 33 2002 827 840.
37. G.T. Stebbins, M.C. Carrillo, J. Dorfman, C. Dirksen, J.E. Desmond, and D.A. Turner et al. Aging effects on memory encoding in the frontal lobes Psychol Aging 17 2002 44 55.
38. G. Kalpouzos, G. Chételat, B. Landeau, P. Clochon, F. Viader, and F. Eustache et al. Structural and metabolic correlates of episodic memory in relation to the depth of encoding in normal aging J Cogn Neurosci 21 2009 372 389.
39. B.A. Kirchhoff, B.A. Anderson, D.M. Barch, and L.L. Jacoby Cognitive and neural effects of semantic encoding strategy training in older adults Cereb Cortex 22 2012 788 799.
40. J. Peña-Casanova, R. Blesa, M. Aguilar, N. Gramunt-Fombuena, B. Gómez-Ansón, and R. Oliva et al. Spanish Multicenter normative studies (NEURONORMA Project): methods and sample characteristics Arch Clin Neuropsychol 24 2009 307 319.
41. E.M. Strauss, D.A. Carone, E.M. Sherman, and O. Spreen A compendium of neuropsychological tests: administration, norms, and commentary Appl Neuropsychol 14 2007 62 63.
42. S. Rossi, M. Hallett, P.M. Rossini, and A. Pascual-Leone Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research Clin Neurophysiol Off J Int Fed Clin Neurophysiol 120 2009 2008 2039.
43. N.S. Gallés, F.C. Vega, M.F.C. Valiña, and M.A.M. Antonin Lexesp - Lexico Informatizado Del Español 2000 Publicacions i Edicions de la Universitat de Barcelona.
44. J.C. Rothwell, M. Hallett, A. Berardelli, A. Eisen, P. Rossini, and W. Paulus Magnetic stimulation: motor evoked potentials. The International Federation of Clinical Neurophysiology Electroencephalogr Clin Neurophysiol Suppl 52 1999 97 103.
45. H. Kim Neural activity that predicts subsequent memory and forgetting: a meta-analysis of 74 fMRI studies NeuroImage 54 2011 2446 2461.
46. M. Jenkinson, and S. Smith A global optimisation method for robust affine registration of brain images Med Image Anal 5 2001 143 156.
47. C.F. Beckmann, M. DeLuca, J.T. Devlin, and S.M. Smith Investigations into resting-state connectivity using independent component analysis Philos Trans R Soc Lond B Biol Sci 360 2005 1001 1013.
48. N. Filippini, B.J. MacIntosh, M.G. Hough, G.M. Goodwin, G.B. Frisoni, and S.M. Smith et al. Distinct patterns of brain activity in young carriers of the APOE-epsilon4 allele Proc Natl Acad Sci U S A 106 2009 7209 7214.
49. T.P. Minka Automatic choice of dimensionality for PCA 2000.
50. C.F. Beckmann, and S.M. Smith Probabilistic independent component analysis for functional magnetic resonance imaging IEEE Trans Med Imaging 23 2004 137 152.
51. J.S. Damoiseaux, S.A.R.B. Rombouts, F. Barkhof, P. Scheltens, C.J. Stam, and S.M. Smith et al. Consistent resting-state networks across healthy subjects Proc Natl Acad Sci U S A 103 2006 13848 13853.
52. B.B. Biswal, M. Mennes, X.-N. Zuo, S. Gohel, C. Kelly, and S.M. Smith et al. Toward discovery science of human brain function Proc Natl Acad Sci U S A 107 2010 4734 4739.
53. T.E. Nichols, and A.P. Holmes Nonparametric permutation tests for functional neuroimaging: a primer with examples Hum Brain Mapp 15 2002 1 25.
54. S.M. Smith, and T.E. Nichols Threshold-free cluster enhancement: addressing problems of smoothing, threshold dependence and localisation in cluster inference NeuroImage 44 2009 83 98.
55. Z. Li, Y. Zhu, A.R. Childress, J.A. Detre, and Z. Wang Relations between BOLD fMRI-derived resting brain activity and cerebral blood flow PloS One 7 2012 e44556.
56. Y.-F. Zang, Y. He, C.-Z. Zhu, Q.-J. Cao, M.-Q. Sui, and M. Liang et al. Altered baseline brain activity in children with ADHD revealed by resting-state functional MRI Brain Dev 29 2007 83 91.
57. Q.-H. Zou, C.-Z. Zhu, Y. Yang, X.-N. Zuo, X.-Y. Long, and Q.-J. Cao et al. An improved approach to detection of amplitude of low-frequency fluctuation (ALFF) for resting-state fMRI: fractional ALFF J Neurosci Methods 172 2008 137 141.
58. M.W. Woolrich, B.D. Ripley, M. Brady, and S.M. Smith Temporal autocorrelation in univariate linear modeling of FMRI data NeuroImage 14 2001 1370 1386.
59. C.F. Beckmann, M. Jenkinson, and S.M. Smith General multilevel linear modeling for group analysis in FMRI NeuroImage 20 2003 1052 1063.
60. K.J. Friston, C. Buechel, G.R. Fink, J. Morris, E. Rolls, and R.J. Dolan Psychophysiological and modulatory interactions in neuroimaging NeuroImage 6 1997 218 229.
61. D.G. McLaren, M.L. Ries, G. Xu, and S.C. Johnson A generalized form of context-dependent psychophysiological interactions (gPPI): a comparison to standard approaches NeuroImage 61 2012 1277 1286.
62. R. Cabeza, N.D. Anderson, J.K. Locantore, and A.R. McIntosh Aging gracefully: compensatory brain activity in high-performing older adults NeuroImage 17 2002 1394 1402.
63. J. Spaniol, and C. Grady Aging and the neural correlates of source memory: over-recruitment and functional reorganization Neurobiol Aging 33 2012 425.e3 425.e18.
64. F. Blankenburg, C.C. Ruff, S. Bestmann, O. Bjoertomt, O. Josephs, and R. Deichmann et al. Studying the role of human parietal cortex in visuospatial attention with concurrent TMS-fMRI Cereb Cortex 20 2010 2702 2711.
65. E. Feredoes, K. Heinen, N. Weiskopf, C. Ruff, and J. Driver Causal evidence for frontal involvement in memory target maintenance by posterior brain areas during distracter interference of visual working memory Proc Natl Acad Sci U S A 108 2011 17510 17515.
66. T. Paus, R. Jech, C.J. Thompson, R. Comeau, T. Peters, and A.C. Evans Transcranial magnetic stimulation during positron emission tomography: a new method for studying connectivity of the human cerebral cortex J Neurosci 17 1997 3178 3184.
67. Y.D. Van der Werf, E.J. Sanz-Arigita, S. Menning, and O.A. van den Heuvel Modulating spontaneous brain activity using repetitive transcranial magnetic stimulation BMC Neurosci 11 2010 145.
68. A. Vercammen, H. Knegtering, E.J. Liemburg, J.A. den Boer, and A. Aleman Functional connectivity of the temporo-parietal region in schizophrenia: effects of rTMS treatment of auditory hallucinations J Psychiatr Res 44 2010 725 731.
69. M.C. Eldaief, M.A. Halko, R.L. Buckner, and A. Pascual-Leone Transcranial magnetic stimulation modulates the brain's intrinsic activity in a frequency-dependent manner Proc Natl Acad Sci U S A 108 2011 21229 21234.
70. R. Polanía, W. Paulus, A. Antal, and M.A. Nitsche Introducing graph theory to track for neuroplastic alterations in the resting human brain: a transcranial direct current stimulation study NeuroImage 54 2011 2287 2296.
71. C. Esslinger, N. Schüler, C. Sauer, D. Gass, D. Mier, and U. Braun et al. Induction and quantification of prefrontal cortical network plasticity using 5 Hz rTMS and fMRI Hum Brain Mapp 35 2014 140 151.
72. L. Cárdenas-Morales, G. Grön, and T. Kammer Exploring the after-effects of theta burst magnetic stimulation on the human motor cortex: a functional imaging study Hum Brain Mapp 32 2011 1948 1960.
73. A.T. Sack, A. Kohler, S. Bestmann, D.E.J. Linden, P. Dechent, and R. Goebel et al. Imaging the brain activity changes underlying impaired visuospatial judgments: simultaneous FMRI, TMS, and behavioral studies Cereb Cortex 17 2007 2841 2852.
74. S. Bestmann, J. Baudewig, and J. Frahm On the synchronization of transcranial magnetic stimulation and functional echo-planar imaging J Magn Reson Imaging 17 2003 309 316.
75. J.S. Simons, and H.J. Spiers Prefrontal and medial temporal lobe interactions in long-term memory Nat Rev Neurosci 4 2003 637 648.
76. E. Jefferies The neural basis of semantic cognition: converging evidence from neuropsychology, neuroimaging and TMS Cortex 49 2013 611 625.
77. J.R. Binder, R.H. Desai, W.W. Graves, and L.L. Conant Where is the semantic system? A critical review and meta-analysis of 120 functional neuroimaging studies Cereb Cortex 19 2009 2767 2796.
78. Y. Song, M. Tian, and J. Liu Top-down processing of symbolic meanings modulates the visual word form area J Neurosci 32 2012 12277 12283.
79. L. Cohen, S. Lehéricy, F. Chochon, C. Lemer, S. Rivaud, and S. Dehaene Language-specific tuning of visual cortex? Functional properties of the Visual Word Form Area Brain J Neurol 125 2002 1054 1069.
80. V. Goffaux, R. Martin, G. Dormal, R. Goebel, and C. Schiltz Attentional shifts induced by uninformative number symbols modulate neural activity in human occipital cortex Neuropsychologia 50 2012 3419 3428.
81. F. Kherif, G. Josse, and C.J. Price Automatic top-down processing explains common left occipito-temporal responses to visual words and objects Cereb Cortex 21 2011 103 114.
82. M. Szwed, E. Qiao, A. Jobert, S. Dehaene, and L. Cohen Effects of literacy in early visual and occipitotemporal areas of Chinese and French readers J Cogn Neurosci 2013.
83. U. Urooj, P.L. Cornelissen, M.I.G. Simpson, K.L. Wheat, W. Woods, and L. Barca et al. Interactions between visual and semantic processing during object recognition revealed by modulatory effects of age of acquisition NeuroImage 87C 2013 252 264.
84. T. Çukur, S. Nishimoto, A.G. Huth, and J.L. Gallant Attention during natural vision warps semantic representation across the human brain Nat Neurosci 16 2013 763 770.
85. F. Pulvermüller, R. Assadollahi, and T. Elbert Neuromagnetic evidence for early semantic access in word recognition Eur J Neurosci 13 2001 201 205.
86. R.L. Moseley, F. Pulvermüller, and Y. Shtyrov Sensorimotor semantics on the spot: brain activity dissociates between conceptual categories within 150 ms Sci Rep 3 2013 1928.
87. M. Kutas, and K.D. Federmeier Thirty years and counting: finding meaning in the N400 component of the event-related brain potential (ERP) Annu Rev Psychol 62 2011 621 647.
88. J. Grafman, A. Pascual-Leone, D. Alway, P. Nichelli, E. Gomez-Tortosa, and M. Hallett Induction of a recall deficit by rapid-rate transcranial magnetic stimulation Neuroreport 5 1994 1157 1160.
89. J. Martino, C. Brogna, S.G. Robles, F. Vergani, and H. Duffau Anatomic dissection of the inferior fronto-occipital fasciculus revisited in the lights of brain stimulation data Cortex 46 2010 691 699.
90. S. Mori, S. Wakana, P.C.M. van Zijl, and L.M. Nagae-Poetscher MRI Atlas of Human White Matter 2005 Elsevier.
91. M.D. Fox, R.L. Buckner, M.P. White, M.D. Greicius, and A. Pascual-Leone Efficacy of transcranial magnetic stimulation targets for depression is related to intrinsic functional connectivity with the subgenual cingulate Biol Psychiatry 72 2012 595 603.
92. T. Higo, R.B. Mars, E.D. Boorman, E.R. Buch, and M.F.S. Rushworth Distributed and causal influence of frontal operculum in task control Proc Natl Acad Sci U S A 108 2011 4230 4235.
93. T.P. Zanto, M.T. Rubens, A. Thangavel, and A. Gazzaley Causal role of the prefrontal cortex in top-down modulation of visual processing and working memory Nat Neurosci 14 2011 656 661.
94. E. Bilek, A. Schäfer, E. Ochs, C. Esslinger, M. Zangl, and M.M. Plichta et al. Application of high-frequency repetitive transcranial magnetic stimulation to the DLPFC alters human prefrontal-hippocampal functional interaction J Neurosci 33 2013 7050 7056.
95. M. Zimerman, K.F. Heise, J. Hoppe, L.G. Cohen, C. Gerloff, and F.C. Hummel Modulation of training by single-session transcranial direct current stimulation to the intact motor cortex enhances motor skill acquisition of the paretic hand Stroke 43 2012 2185 2191.