Age-related changes in the somatosensory processing of tactile stimulation-An fMRI study

Behavioural Brain Research

Volumn 238, Issue 1, 2013, Pages 259-264

  Brodoehl, Stefan ^a   Klingner, Carsten ^a   Stieglitz, Katharina ^a   Witte, Otto W ^a  

^a FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

Author keywords

Age related; BOLD signal; Current perception threshold; FMRI; Inhibition; Somatosensory cortex

Indexed keywords

ADULT; AGE; AGED; ANTERIOR CINGULATE; ARTICLE; BOLD SIGNAL; BRAIN REGION; CONTROLLED STUDY; CORPUS CALLOSUM; EVOKED RESPONSE; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HUMAN EXPERIMENT; MALE; MENTAL TASK; MOTOR CORTEX; NERVE CELL NETWORK; NEUROIMAGING; PERCEPTIVE THRESHOLD; POSTERIOR CINGULATE; PRIORITY JOURNAL; RIGHT HANDEDNESS; SOMATOSENSORY SYSTEM; TACTILE STIMULATION; TASK PERFORMANCE;

ADULT; AGED; AGING; BRAIN; BRAIN MAPPING; FEMALE; FUNCTIONAL NEUROIMAGING; HAND; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; PHYSICAL STIMULATION; SENSORY THRESHOLDS; SOMATOSENSORY CORTEX; TOUCH; TOUCH PERCEPTION;

EID: 84868692039     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2012.10.038     Document Type: Article

References (78)

1. Cabeza R. Hemispheric asymmetry reduction in older adults: the HAROLD model. Psychology and Aging 2002, 17:85-100.
2. Raz N., Lindenberger U., Rodrigue K.M., Kennedy K.M., Head D., Williamson A., et al. Regional brain changes in aging healthy adults: general trends, individual differences and modifiers. Cerebral Cortex 2005, 15:1676-1689.
3. D'Esposito M., Zarahn E., Aguirre G.K., Rypma B. The effect of normal aging on the coupling of neural activity to the bold hemodynamic response. Neuroimage 1999, 10:6-14.
4. 15O and positron emission tomography: theory, procedure, and normal values. Journal of Computer Assisted Tomography 1980, 4:727-736.
5. Leenders K.L., Perani D., Lammertsma A.A., Heather J.D., Buckingham P., Healy M.J. Cerebral blood flow, blood volume and oxygen utilization, normal values and effect of age. Brain 1990, 113(Pt 1):27-47.
6. Riecker A., Grodd W., Klose U., Schulz J.B., Groschel K., Erb M., et al. Relation between regional functional MRI activation and vascular reactivity to carbon dioxide during normal aging. Journal of Cerebral Blood Flow and Metabolism 2003, 23:565-573.
7. Marchal G., Rioux P., Petit-Taboue M.C., Sette G., Travere J.M., Le Poec C., et al. Regional cerebral oxygen consumption, blood flow, and blood volume in healthy human aging. Archives of Neurology 1992, 49:1013-1020.
8. Martin A.J., Friston K.J., Colebatch J.G., Frackowiak R.S. Decreases in regional cerebral blood flow with normal aging. Journal of Cerebral Blood Flow and Metabolism 1991, 11:684-689.
9. Long J.M., Mouton P.R., Jucker M., Ingram D.K. What counts in brain aging? Design-based stereological analysis of cell number. The Journals of Gerontology Series A: Biological Sciences and Medical Sciences 1999, 54:B407-B417.
10. Terry R.D., DeTeresa R., Hansen L.A. Neocortical cell counts in normal human adult aging. Annals of Neurology 1987, 21:530-539.
11. Mayhan W.G., Faraci F.M., Baumbach G.L., Heistad D.D. Effects of aging on responses of cerebral arterioles. American Journal of Physiology 1990, 258:H1138-H1143.
12. Raichle M.E., MacLeod A.M., Snyder A.Z., Powers W.J., Gusnard D.A., Shulman G.L. A default mode of brain function. Proceedings of National Academy of Sciences of the United States of America 2001, 98:676-682.
13. Fox M.D., Snyder A.Z., Vincent J.L., Corbetta M., Van Essen D.C., Raichle M.E. The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proceedings of National Academy of Sciences of the United States of America 2005, 102:9673-9678.
14. Grady C.L., Protzner A.B., Kovacevic N., Strother S.C., Afshin-Pour B., Wojtowicz M., et al. A multivariate analysis of age-related differences in default mode and task-positive networks across multiple cognitive domains. Cerebral Cortex 2010, 20:1432-1447.
15. Lustig C., Snyder A.Z., Bhakta M., O'Brien K.C., McAvoy M., Raichle M.E., et al. Functional deactivations: change with age and dementia of the Alzheimer type. Proceedings of National Academy of Sciences of the United States of America 2003, 100:14504-14509.
16. Peiffer A.M., Hugenschmidt C.E., Maldjian J.A., Casanova R., Srikanth R., Hayasaka S., et al. Aging and the interaction of sensory cortical function and structure. Human Brain Mapping 2009, 30:228-240.
17. Ross M.H., Yurgelun-Todd D.A., Renshaw P.F., Maas L.C., Mendelson J.H., Mello N.K., et al. Age-related reduction in functional MRI response to photic stimulation. Neurology 1997, 48:173-176.
18. Yousem D.M., Maldjian J.A., Hummel T., Alsop D.C., Geckle R.J., Kraut M.A., et al. The effect of age on odor-stimulated functional MR imaging. AJNR American Journal of Neuroradiology 1999, 20:600-608.
19. Goble D.J., Coxon J.P., Van Impe A., Geurts M., Van Hecke W., Sunaert S., et al. The neural basis of central proprioceptive processing in older versus younger adults: An important sensory role for right putamen. Human Brain Mapping 2011, 33(4):895-908.
20. Hesselmann V., Zaro Weber O., Wedekind C., Krings T., Schulte O., Kugel H., et al. Age related signal decrease in functional magnetic resonance imaging during motor stimulation in humans. Neuroscience Letters 2001, 308:141-144.
21. Voss M.W., Erickson K.I., Chaddock L., Prakash R.S., Colcombe S.J., Morris K.S., et al. Dedifferentiation in the visual cortex: an fMRI investigation of individual differences in older adults. Brain Research 2008, 1244:121-131.
22. Park D.C., Polk T.A., Park R., Minear M., Savage A., Smith M.R. Aging reduces neural specialization in ventral visual cortex. Proceedings of National Academy of Sciences of the United States of America 2004, 101:13091-13095.
23. Kalisch T., Ragert P., Schwenkreis P., Dinse H.R., Tegenthoff M. Impaired tactile acuity in old age is accompanied by enlarged hand representations in somatosensory cortex. Cerebral Cortex 2009, 19:1530-1538.
24. Payer D., Marshuetz C., Sutton B., Hebrank A., Welsh R.C., Park D.C. Decreased neural specialization in old adults on a working memory task. Neuroreport 2006, 17:487-491.
25. Spaniol J., Grady C. Aging and the neural correlates of source memory: over-recruitment and functional reorganization. Neurobiology of Aging 2012, 33:425 e3-e425018.
26. Loibl M., Beutling W., Kaza E., Lotze M. Non-effective increase of fMRI-activation for motor performance in elder individuals. Behavioural Brain Research 2011, 223:280-286.
27. Riecker A., Groschel K., Ackermann H., Steinbrink C., Witte O., Kastrup A. Functional significance of age-related differences in motor activation patterns. Neuroimage 2006, 32:1345-1354.
28. Malandraki G.A., Perlman A.L., Karampinos D.C., Sutton B.P. Reduced somatosensory activations in swallowing with age. Human Brain Mapping 2011, 32:730-743.
29. Teismann I.K., Steinstraeter O., Schwindt W., Ringelstein E.B., Pantev C., Dziewas R. Age-related changes in cortical swallowing processing. Neurobiology of Aging 2010, 31:1044-1050.
30. Backes W.H., Mess W.H., van Kranen-Mastenbroek V., Reulen J.P. Somatosensory cortex responses to median nerve stimulation: fMRI effects of current amplitude and selective attention. Clinical Neurophysiology 2000, 111:1738-1744.
31. Kawamura T., Nakasato N., Seki K., Kanno A., Fujita S., Fujiwara S., et al. Neuromagnetic evidence of pre- and post-central cortical sources of somatosensory evoked responses. Electroencephalography and Clinical Neurophysiology 1996, 100:44-50.
32. Huttunen J., Wikstrom H., Salonen O., Ilmoniemi R.J. Human somatosensory cortical activation strengths: comparison between males and females and age-related changes. Brain Research 1999, 818:196-203.
33. Stephen J.M., Ranken D., Best E., Adair J., Knoefel J., Kovacevic S., et al. Aging changes and gender differences in response to median nerve stimulation measured with MEG. Clinical Neurophysiology 2006, 117:131-143.
34. Lenz M., Tegenthoff M., Kohlhaas K., Stude P., Hoffken O., Gatica Tossi M.A., et al. Increased excitability of somatosensory cortex in aged humans is associated with impaired tactile acuity. Journal of Neuroscience 2012, 32:1811-1816.
35. Folstein M.F., Folstein S.E., McHugh P.R. Mini-mental state, a practical method for grading the cognitive state of patients for the clinician. Journal of Psychiatric Research 1975, 12:189-198.
36. Evans E.R., Rendell M.S., Bartek J.P., Bamisedun O., Connor S., Giitter M. Current perception thresholds in ageing. Age and Ageing 1992, 21:273-279.
37. Perret E., Regli F. Age and the perceptual threshold for vibratory stimuli. European Neurology 1970, 4:65-76.
38. Sherman E.D., Robillard E. Sensitivity to pain in the aged. Canadian Medical Association Journal 1960, 83:944-947.
39. Tseng C.H., Faca Tseng C.P., Chong C.K. Aging and current perception threshold measured by neurometer in normal Taiwanese adults. Journal of the American Geriatrics Society 2002, 50:2094-2095.
40. Kiebel S.J., Ashburner J., Poline J.B., Friston K.J. MRI and PET coregistration - a cross validation of statistical parametric mapping and automated image registration. Neuroimage 1997, 5:271-279.
41. Friston K.J., Ashburner J., Frith C.D., Poline J.B., Heather J.D., Frackowiak R.S.J. Spatial registration and normalization of images. Human Brain Mapping 1995, 3:165-189.
42. Evans A.C., Collins D.L., Mills S.R., Brown E.D., Kelly R.L., Peters T.M. Nuclear science symposium and medical imaging conference, 1993 IEEE Conference Record, vol. 3 1993, 1813-1817.
43. Eickhoff S.B., Schleicher A., Zilles K., Amunts K. The human parietal operculum. I. Cytoarchitectonic mapping of subdivisions. Cerebral Cortex 2006, 16:254-267.
44. Eickhoff S.B., Stephan K.E., Mohlberg H., Grefkes C., Fink G.R., Amunts K., et al. A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. Neuroimage 2005, 25:1325-1335.
45. Genovese C.R., Lazar N.A., Nichols T. Thresholding of statistical maps in functional neuroimaging using the false discovery rate. Neuroimage 2002, 15:870-878.
46. Lindquist M.A., Wager T.D. Validity and power in hemodynamic response modeling: a comparison study and a new approach. Human Brain Mapping 2007, 28:764-784.
47. Klingner C.M., Hasler C., Brodoehl S., Witte O.W. Dependence of the negative BOLD response on somatosensory stimulus intensity. Neuroimage 2010, 53:189-195.
48. Klingner C.M., Ebenau K., Hasler C., Brodoehl S., Gorlich Y., Witte O.W. Influences of negative BOLD responses on positive BOLD responses. Neuroimage 2011, 55:1709-1715.
49. Deuchert M., Ruben J., Schwiemann J., Meyer R., Thees S., Krause T., et al. Event-related fMRI of the somatosensory system using electrical finger stimulation. Neuroreport 2002, 13:365-369.
50. Karhu J., Tesche C.D. Simultaneous early processing of sensory input in human primary (SI) and secondary (SII) somatosensory cortices. Journal of Neurophysiology 1999, 81:2017-2025.
51. Ruben J., Krause T., Taskin B., Blankenburg F., Moosmann M., Villringer A. Sub-area-specific suppressive interaction in the BOLD responses to simultaneous finger stimulation in human primary somatosensory cortex: evidence for increasing rostral-to-caudal convergence. Cerebral Cortex 2006, 16:819-826.
52. Klingner C.M., Nenadic I., Hasler C., Brodoehl S., Witte O.W. Habituation within the somatosensory processing hierarchy. Behavioural Brain Research 2011, 225:432-436.
53. Cramp F.L., McCullough G.R., Lowe A.S., Walsh D.M. Transcutaneous electric nerve stimulation: the effect of intensity on local and distal cutaneous blood flow and skin temperature in healthy subjects. Archives of Physical Medicine and Rehabilitation 2002, 83:5-9.
54. Burke D., Gandevia S.C. Interfering cutaneous stimulation and the muscle afferent contribution to cortical potentials. Electroencephalography and Clinical Neurophysiology 1988, 70:118-125.
55. Dean J., Bowsher D., Johnson M.I. The effects of unilateral transcutaneous electrical nerve stimulation of the median nerve on bilateral somatosensory thresholds. Clinical Physiology and Functional Imaging 2006, 26:314-318.
56. Bruce M.F. The relation of tactile thresholds to histology in the fingers of elderly people. Journal of Neurology, Neurosurgery, and Psychiatry 1980, 43:730-734.
57. Dorfman L.J., Bosley T.M. Age-related changes in peripheral and central nerve conduction in man. Neurology 1979, 29:38-44.
58. Lin Y.Y., Shih Y.H., Chen J.T., Hsieh J.C., Yeh T.C., Liao K.K., et al. Differential effects of stimulus intensity on peripheral and neuromagnetic cortical responses to median nerve stimulation. Neuroimage 2003, 20:909-917.
59. Zhang N., Gore J.C., Chen L.M., Avison M.J. Dependence of BOLD signal change on tactile stimulus intensity in SI of primates. Magnetic Resonance Imaging 2007, 25:784-794.
60. Schmidt S., Redecker C., Bruehl C., Witte O.W. Age-related decline of functional inhibition in rat cortex. Neurobiology of Aging 2010, 31:504-511.
61. Schmolesky M.T., Wang Y., Pu M., Leventhal A.G. Degradation of stimulus selectivity of visual cortical cells in senescent rhesus monkeys. Nature Neuroscience 2000, 3:384-390.
62. Buzsaki G., Kaila K., Raichle M. Inhibition and brain work. Neuron 2007, 56:771-783.
63. 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.
64. Shulman R.G., Rothman D.L., Behar K.L., Hyder F. Energetic basis of brain activity: implications for neuroimaging. Trends in Neurosciences 2004, 27:489-495.
65. Ames A. CNS energy metabolism as related to function. Brain Research Reviews 2000, 34:42-68.
66. Paulson O.B., Hasselbalch S.G., Rostrup E., Knudsen G.M., Pelligrino D. Cerebral blood flow response to functional activation. Journal of Cerebral Blood Flow and Metabolism 2010, 30:2-14.
67. Poe B.H., Linville C., Brunso-Bechtold J. Age-related decline of presumptive inhibitory synapses in the sensorimotor cortex as revealed by the physical disector. The Journal of Comparative Neurology 2001, 439:65-72.
68. Peinemann A., Lehner C., Conrad B., Siebner H.R. Age-related decrease in paired-pulse intracortical inhibition in the human primary motor cortex. Neuroscience Letters 2001, 313:33-36.
69. Godde B., Berkefeld T., David-Jurgens M., Dinse H.R. Age-related changes in primary somatosensory cortex of rats: evidence for parallel degenerative and plastic-adaptive processes. Neuroscience and Biobehavioral Reviews 2002, 26:743-752.
70. Brunso-Bechtold J.K., Linville M.C., Sonntag W.E. Age-related synaptic changes in sensorimotor cortex of the Brown Norway X Fischer 344 rat. Brain Research 2000, 872:125-133.
71. Talelli P., Waddingham W., Ewas A., Rothwell J.C., Ward N.S. The effect of age on task-related modulation of interhemispheric balance. Experimental Brain Research 2008, 186:59-66.
72. Ferbert A., Priori A., Rothwell J.C., Day B.L., Colebatch J.G., Marsden C.D. Interhemispheric inhibition of the human motor cortex. Journal of Psychology 1992, 453:525-546.
73. Grady C.L. Functional brain imaging and age-related changes in cognition. Biological Psychology 2000, 54:259-281.
74. Kokmen E., Bossemeyer R.W., Barney J., Williams W.J. Neurological manifestations of aging. Journal of Gerontology 1977, 32:411-419.
75. Valeriani M., Ranghi F., Giaquinto S. The effects of aging on selective attention to touch: a reduced inhibitory control in elderly subjects. International Journal of Psychophysiology 2003, 49:75-87.
76. Wu J.T., Wu H.Z., Yan C.G., Chen W.X., Zhang H.Y., He Y., et al. Aging-related changes in the default mode network and its anti-correlated networks: a resting-state fMRI study. Neuroscience Letters 2011, 504:62-67.
77. 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.
78. Gusnard D.A., Akbudak E., Shulman G.L., Raichle M.E. Medial prefrontal cortex and self-referential mental activity: relation to a default mode of brain function. Proceedings of National Academy of Sciences of the United States of America 2001, 98:4259-4264.