A simultaneous ERP/fMRI investigation of the P300 aging effect

Neurobiology of Aging

Volumn 33, Issue 10, 2012, Pages 2448-2461

  O'Connell, Redmond G ^a   Balsters, Joshua H ^a   Kilcullen, Sophia M ^a   Campbell, William ^a   Bokde, Arun W ^a   Lai, Robert ^b   Upton, Neil ^b   Robertson, Ian H ^a  

^a TRINITY COLLEGE DUBLIN   (Ireland)

^b GLAXOSMITHKLINE   (United Kingdom)

Author keywords

Aging; Distractor processing; EEG; FMRI; Frontal; P300; Target processing

Indexed keywords

ADULT; AGED; AGING; ARTICLE; BRAIN DEPTH RECORDING; BRAIN DEPTH STIMULATION; BRAIN REGION; CINGULATE GYRUS; CONTROLLED STUDY; ELECTRODE; ELECTROENCEPHALOGRAPHY; EVENT RELATED POTENTIAL; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HIPPOCAMPUS; HUMAN; HUMAN EXPERIMENT; MALE; MENTAL TASK; NERVE POTENTIAL; NEUROIMAGING; NORMAL HUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; RESPONSE TIME; TASK PERFORMANCE; VISUAL STIMULATION;

ADOLESCENT; ADULT; AGED; AGING; CEREBRAL CORTEX; ELECTROENCEPHALOGRAPHY; EVENT-RELATED POTENTIALS, P300; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; PSYCHOMOTOR PERFORMANCE; REACTION TIME; YOUNG ADULT;

EID: 84864389345     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2011.12.021     Document Type: Article

References (71)

1. Aguirre G.K., Zarahn E., D'Esposito M. The variability of human, BOLD hemodynamic responses. Neuroimage 1998, 8:360-369.
2. Allen P.J., Josephs O., Turner R. A method for removing imaging artifact from continuous EEG recorded during functional MRI. Neuroimage 2000, 12:230-239.
3. Allen P.J., Polizzi G., Krakow K., Fish D.R., Lemieux L. Identification of EEG events in the MR scanner: the problem of pulse artifact and a method for its subtraction. Neuroimage 1998, 8:229-239.
4. Andersson J.L., Hutton C., Ashburner J., Turner R., Friston K. Modeling geometric deformations in EPI time series. Neuroimage 2001, 13:903-919.
5. Aron A.R., Poldrack R.A. The cognitive neuroscience of response inhibition: relevance for genetic research in attention-deficit/hyperactivity disorder. Biol. Psychiatry 2005, 57:1285-1292.
6. Ashburner J., Friston K.J. Unified segmentation. Neuroimage 2005, 26:839-851.
7. Balsters J.H., Ramnani N. Symbolic representations of action in the human cerebellum. Neuroimage 2008, 43:388-398.
8. Ben-Simon E., Podlipsky I., Arieli A., Zhdanov A., Hendler T. Never resting brain: simultaneous representation of two alpha related processes in humans. PLoS One 2008, 3:e3984.
9. Bledowski C., Prvulovic D., Goebel R., Zanella F.E., Linden D.E. Attentional systems in target and distractor processing: a combined ERP and fMRI study. Neuroimage 2004, 22:530-540.
10. Cabeza R., Anderson N.D., Locantore J.K., McIntosh A.R. Aging gracefully: compensatory brain activity in high-performing older adults. Neuroimage 2002, 17:1394-1402.
11. Convit A., De Leon M.J., Tarshish C., De Santi S., Tsui W., Rusinek H., George A. Specific hippocampal volume reductions in individuals at risk for Alzheimer's disease. Neurobiol. Aging 1997, 18:131-138.
12. D'Esposito M., Deouell L.Y., Gazzaley A. Alterations in the BOLD fMRI signal with ageing and disease: a challenge for neuroimaging. Nat. Rev. Neurosci 2003, 4:863-872.
13. Davis S.W., Dennis N.A., Daselaar S.M., Fleck M.S., Cabeza R. Que PASA?. The posterior-anterior shift in aging. Cereb. Cortex 2008, 18:1201-1209.
14. De Sanctis P., Katz R., Wylie G.R., Sehatpour P., Alexopoulos G.S., Foxe J.J. Enhanced and bilateralized visual sensory processing in the ventral stream may be a feature of normal aging. Neurobiol. Aging 2008, 29:1576-1586.
15. Debener S., Mullinger K.J., Niazy R.K., Bowtell R.W. Properties of the ballistocardiogram artefact as revealed by EEG recordings at 1.5, 3 and 7 T static magnetic field strength. Int. J. Psychophysiol 2008, 67:189-199.
16. Debener S., Strobel A., Sorger B., Peters J., Kranczioch C., Engel A.K., Goebel R. Improved quality of auditory event-related potentials recorded simultaneously with 3-T fMRI: removal of the ballistocardiogram artefact. Neuroimage 2007, 34:587-597.
17. Debener S., Ullsperger M., Siegel M., Fiehler K., von Cramon D.Y., Engel A.K. Trial-by-trial coupling of concurrent electroencephalogram and functional magnetic resonance imaging identifies the dynamics of performance monitoring. J. Neurosci 2005, 25:11730-11737.
18. Debettencourt M., Goldman R., Brown T., Sajda P. Adaptive thresholding for improving sensitivity in single-trial simultaneous EEG/FMRI. Front. Psychol 2011, 2:91.
19. Dockree P.M., Kelly S.P., Robertson I.H., Reilly R.B., Foxe J.J. Neurophysiological markers of alert responding during goal-directed behavior: a high-density electrical mapping study. Neuroimage 2005, 27:587-601.
20. Donchin E. Presidential address, 1980. Surprise!...Surprise?. Psychophysiology 1981, 18:493-513.
21. Eichele T., Specht K., Moosmann M., Jongsma M.L., Quiroga R.Q., Nordby H., Hugdahl K. Assessing the spatiotemporal evolution of neuronal activation with single-trial event-related potentials and functional MRI. Proc. Natl. Acad. Sci. U. S. A 2005, 102:17798-17803.
22. Fabiani M., Friedman D. Changes in brain activity patterns in aging: The novelty oddball. Psychophysiology 1995, 32:579-594.
23. Fabiani M., Friedman D., Cheng J.C. Individual differences in P3 scalp distribution in older adults, and their relationship to frontal lobe function. Psychophysiology 1998, 35:698-708.
24. Falkenstein M., Yordanova J., Kolev V. Effects of aging on slowing of motor-response generation. Int. J. Psychophysiol 2006, 59:22-29.
25. Finnigan S., O'Connell R.G., Cummins T.D., Broughton M., Robertson I.H. ERP measures indicate both attention and working memory encoding decrements in aging. Psychophysiology 2011, 48:601-611.
26. Fjell A.M., Walhovd K.B. Life-span changes in P3a. Psychophysiology 2004, 41:575-583.
27. Friedman D. Cognition and aging: a highly selective overview of event-related potential (ERP) data. J. Clin. Exp. Neuropsychol 2003, 25:702-720.
28. Friston K.J., Frith C.D., Frackowiak R.S., Turner R. Characterizing dynamic brain responses with fMRI: a multivariate approach. Neuroimage 1995, 2:166-172.
29. Friston K.J., Frith C.D., Turner R., Frackowiak R.S. Characterizing evoked hemodynamics with fMRI. Neuroimage 1995, 2:157-165.
30. Goh J.O., Park D.C. Neuroplasticity and cognitive aging: The scaffolding theory of aging and cognition. Restor. Neurol. Neurosci 2009, 27:391-403.
31. Gunning-Dixon F.M., Raz N. Neuroanatomical correlates of selected executive functions in middle-aged and older adults: a prospective MRI study. Neuropsychologia 2003, 41:1929-1941.
32. Halgren E., Baudena P., Clarke J.M., Heit G., Marinkovic K., Devaux B., Vignal J.P., Biraben A. Intracerebral potentials to rare target and distractor auditory and visual stimuli. II. Medial, lateral and posterior temporal lobe. Electroencephalogr. Clin. Neurophysiol 1995, 94:229-250.
33. Handwerker D.A., Ollinger J.M., D'Esposito M. Variation of BOLD hemodynamic responses across subjects and brain regions and their effects on statistical analyses. Neuroimage 2004, 21:1639-1651.
34. Huster R.J., Eichele T., Enriquez-Geppert S., Wollbrink A., Kugel H., Konrad C., Pantev C. Multimodal imaging of functional networks and event-related potentials in performance monitoring. Neuroimage 2011, 56:1588-1597.
35. Hutton C., Bork A., Josephs O., Deichmann R., Ashburner J., Turner R. Image distortion correction in fMRI: A quantitative evaluation. Neuroimage 2002, 16:217-240.
36. Iannetti G.D., Niazy R.K., Wise R.G., Jezzard P., Brooks J.C., Zambreanu L., Vennart W., Matthews P.M., Tracey I. Simultaneous recording of laser-evoked brain potentials and continuous, high-field functional magnetic resonance imaging in humans. Neuroimage 2005, 28:708-719.
37. Kannurpatti S.S., Motes M.A., Rypma B., Biswal B.B. Neural and vascular variability and the fMRI-BOLD response in normal aging. Magn. Reson. Imaging 2010, 28:466-476.
38. Karch S., Feuerecker R., Leicht G., Meindl T., Hantschk I., Kirsch V., Ertl M., Lutz J., Pogarell O., Mulert C. Separating distinct aspects of the voluntary selection between response alternatives: N2- and P3-related BOLD responses. Neuroimage 2010, 51:356-364.
39. Kelly A.M., Garavan H. Human functional neuroimaging of brain changes associated with practice. Cereb. Cortex 2005, 15:1089-1102.
40. Kiehl K.A., Laurens K.R., Duty T.L., Forster B.B., Liddle P.F. Neural sources involved in auditory target detection and novelty processing: an event-related fMRI study. Psychophysiology 2001, 38:133-142.
41. Kirino E., Belger A., Goldman-Rakic P., McCarthy G. Prefrontal activation evoked by infrequent target and novel stimuli in a visual target detection task: an event-related functional magnetic resonance imaging study. J. Neurosci 2000, 20:6612-6618.
42. Knight R. Contribution of human hippocampal region to novelty detection. Nature 1996, 383:256-259.
43. Linden D.E. The p300: where in the brain is it produced and what does it tell us?. Neuroscientist 2005, 11:563-576.
44. Logothetis N.K., Pauls J., Augath M., Trinath T., Oeltermann A. Neurophysiological investigation of the basis of the fMRI signal. Nature 2001, 412:150-157.
45. Madden D.J., Spaniol J., Whiting W.L., Bucur B., Provenzale J.M., Cabeza R., White L.E., Huettel S.A. Adult age differences in the functional neuroanatomy of visual attention: a combined fMRI and DTI study. Neurobiol. Aging 2007, 28:459-476.
46. Madden D.J., Whiting W.L., Provenzale J.M., Huettel S.A. Age-related changes in neural activity during visual target detection measured by fMRI. Cereb. Cortex 2004, 14:143-155.
47. Mantini D., Corbetta M., Perrucci M.G., Romani G.L., Del Gratta C. Large-scale brain networks account for sustained and transient activity during target detection. Neuroimage 2009, 44:265-274.
48. McCarthy G., Wood C.C., Williamson P.D., Spencer D.D. Task-dependent field potentials in human hippocampal formation. J. Neurosci 1989, 9:4253-4268.
49. McDermott K.B., Petersen S.E., Watson J.M., Ojemann J.G. A procedure for identifying regions preferentially activated by attention to semantic and phonological relations using functional magnetic resonance imaging. Neuropsychologia 2003, 41:293-303.
50. Mullinger K.J., Morgan P.S., Bowtell R.W. Improved artifact correction for combined electroencephalography/functional MRI by means of synchronization and use of vectorcardiogram recordings. J. Magn. Reson. Imaging 2008, 27:607-616.
51. Nieuwenhuis S., Aston-Jones G., Cohen J.D. Decision making, the P3, and the locus coeruleus-norepinephrine system. Psychol. Bull 2005, 131:510-532.
52. Novitskiy N., Ramautar J.R., Vanderperren K., De Vos M., Mennes M., Mijovic B., Vanrumste B., Stiers P., Van den Bergh B., Lagae L., Sunaert S., Van Huffel S., Wagemans J. The BOLD correlates of the visual P1 and N1 in single-trial analysis of simultaneous EEG-fMRI recordings during a spatial detection task. Neuroimage 2011, 54:824-835.
53. Polich J. On the relationship between EEG and P300: individual differences, aging, and ultradian rhythms. Int. J. Psychophysiol 1997, 26:299-317.
54. Polich J. Updating P300: an integrative theory of P3a and P3b. Clin. Neurophysiol 2007, 118:2128-2148.
55. Polich J., Criado J.R. Neuropsychology and neuropharmacology of P3a and P3b. Int. J. Psychophysiol 2006, 60:172-185.
56. Quian Quiroga R., Garcia H. Single-trial event-related potentials with wavelet denoising. Clin. Neurophysiol 2003, 114:376-390.
57. Raz N. Aging of the brain and its impact on cognitive performance: Integration of structural and functional findings. Handbook of Aging and Cognition 2000, 1-90. Erlbaum, Mahwah, NJ. second ed. F.I.M. Craik, T.A. Salthouse (Eds.).
58. Raz N., Lindenberger U., Rodrigue K.M., Kennedy K.M., Head D., Williamson A., Dahle C., Gerstorf D., Acker J.D. Regional brain changes in aging healthy adults: general trends, individual differences and modifiers. Cereb. Cortex 2005, 15:1676-1689.
59. Richardson C., Bucks R.S., Hogan A.M. Effects of aging on habituation to novelty: An ERP study. Int. J. Psychophysiol 2011, 79:97-105.
60. Rossini P.M., Rossi S., Babiloni C., Polich J. Clinical neurophysiology of aging brain: from normal aging to neurodegeneration. Prog. Neurobiol 2007, 83:375-400.
61. Snyder E., Hillyard S.A. Long-latency evoked potentials to irrelevant, deviant stimuli. Behav. Biol 1976, 16:319-331.
62. Solbakk A.K., Fuhrmann Alpert G., Furst A.J., Hale L.A., Oga T., Chetty S., Pickard N., Knight R.T. Altered prefrontal function with aging: insights into age-associated performance decline. Brain Res 2008, 1232:30-47.
63. Strobel A., Debener S., Sorger B., Peters J.C., Kranczioch C., Hoechstetter K., Engel A.K., Brocke B., Goebel R. Novelty and target processing during an auditory novelty oddball: a simultaneous event-related potential and functional magnetic resonance imaging study. Neuroimage 2008, 40:869-883.
64. Sutton S., Braren M., Zubin J., John E.R. Evoked-potential correlates of stimulus uncertainty. Science 1965, 150:1187-1188.
65. Tekin S., Cummings J.L. Frontal-subcortical neuronal circuits and clinical neuropsychiatry: an update. J. Psychosom. Res 2002, 53:647-654.
66. Verleger R. P3b: towards some decision about memory. Clin. Neurophysiol 2008, 119:968-970.
67. Warbrick T., Mobascher A., Brinkmeyer J., Musso F., Richter N., Stoecker T., Fink G.R., Shah N.J., Winterer G. Single-trial P3 amplitude and latency informed event-related fMRI models yield different BOLD response patterns to a target detection task. Neuroimage 2009, 47:1532-1544.
68. West R., Schwarb H., Johnson B.N. The influence of age and individual differences in executive function on stimulus processing in the oddball task. Cortex 2010, 46:550-563.
69. Wylie G.R., Javitt D.C., Foxe J.J. Task switching: a high-density electrical mapping study. Neuroimage 2003, 20:2322-2342.
70. Yamaguchi S., Hale L.A., D'Esposito M., Knight R.T. Rapid prefrontal-hippocampal habituation to novel events. J. Neurosci 2004, 24:5356-5363.
71. Ystad M.A., Lundervold A.J., Wehling E., Espeseth T., Rootwelt H., Westlye L.T., Andersson M., Adolfsdottir S., Geitung J.T., Fjell A.M., Reinvang I., Lundervold A. Hippocampal volumes are important predictors for memory function in elderly women. BMC Med. Imaging 2009, 9:17.