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

Age-related changes in brain function are complex. Although ageing is associated with a reduction in cerebral blood flow and neuronal activity, task-related processing is often correlated with an enlargement of the corresponding and additionally recruited brain areas. This supplemental employment is considered an attempt to compensate for deficits in the ageing brain. Although there are contradictory reports regarding the role of the primary somatosensory cortex (SI), currently, there is little knowledge about age-related functional changes in other brain areas in the somatosensory network (secondary somatosensory cortex (SII), and insular, anterior (ACC) and posterior cingulate cortices (PCC)). We investigated 16 elderly (age range, 62-71 years) and 18 young subjects (age range, 21-28 years) by determining the current perception threshold (CPT) and applying functional magnetic resonance imaging (fMRI) using a 3.0 Tesla scanner under tactile stimulation of the right hand. CPT was positively correlated with age. fMRI analysis revealed significantly increased activation in the contralateral SI and ipsilateral motor cortex in elderly subjects. Furthermore, we demonstrated age-related reductions in the activity in the SII, ACC, PCC, and dorsal parts of the corpus callosum. Our study revealed dramatic age-related differences in the processing of a simple tactile stimulus in the somatosensory network. Specifically, we detected enhanced activation in the contralateral SI and ipsilateral motor cortex assumingly caused by deficient inhibition and decreased activation in later stages of somatosensory processing (SII, cingulate cortex) in elderly subjects. These results indicate that, in addition to over-activation to compensate for impaired brain functions, there are complex mechanisms of modified inhibition and excitability involved in somatosensory processing in the ageing brain.

[1]  S. Swinnen,et al.  The neural basis of central proprioceptive processing in older versus younger adults: An important sensory role for right putamen , 2012, Human brain mapping.

[2]  T. Yoshimoto,et al.  Neuromagnetic evidence of pre- and post-central cortical sources of somatosensory evoked responses. , 1996, Electroencephalography and clinical neurophysiology.

[3]  Karl J. Friston,et al.  MRI and PET Coregistration—A Cross Validation of Statistical Parametric Mapping and Automated Image Registration , 1997, NeuroImage.

[4]  Thomas Berkefeld,et al.  Age-related changes in primary somatosensory cortex of rats: evidence for parallel degenerative and plastic-adaptive processes , 2002, Neuroscience & Biobehavioral Reviews.

[5]  Karl J. Friston,et al.  Spatial registration and normalization of images , 1995 .

[6]  Tzu-Chen Yeh,et al.  Differential effects of stimulus intensity on peripheral and neuromagnetic cortical responses to median nerve stimulation , 2003, NeuroImage.

[7]  D K Ingram,et al.  What counts in brain aging? Design-based stereological analysis of cell number. , 1999, The journals of gerontology. Series A, Biological sciences and medical sciences.

[8]  Denise C. Park,et al.  Aging reduces neural specialization in ventral visual cortex. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[9]  R. Cabeza Hemispheric asymmetry reduction in older adults: the HAROLD model. , 2002, Psychology and aging.

[10]  Mark I. Johnson,et al.  The effects of unilateral transcutaneous electrical nerve stimulation of the median nerve on bilateral somatosensory thresholds , 2006, Clinical physiology and functional imaging.

[11]  C. Grady Functional brain imaging and age-related changes in cognition , 2000, Biological Psychology.

[12]  R. J. Ilmoniemi,et al.  Human somatosensory cortical activation strengths: comparison between males and females and age-related changes , 1999, Brain Research.

[13]  N. Logothetis,et al.  Neurophysiological investigation of the basis of the fMRI signal , 2001, Nature.

[14]  J. Morris,et al.  Functional deactivations: Change with age and dementia of the Alzheimer type , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[15]  B. Day,et al.  Interhemispheric inhibition of the human motor cortex. , 1992, The Journal of physiology.

[16]  Egill Rostrup,et al.  Cerebral Blood Flow Response to Functional Activation , 2010, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[17]  F. Regli,et al.  Age and the perceptual threshold for vibratory stimuli. , 1970, European neurology.

[18]  Cheryl L. Dahle,et al.  Regional brain changes in aging healthy adults: general trends, individual differences and modifiers. , 2005, Cerebral cortex.

[19]  Julia Spaniol,et al.  Aging and the neural correlates of source memory: over-recruitment and functional reorganization , 2012, Neurobiology of Aging.

[20]  S C Gandevia,et al.  Interfering cutaneous stimulation and the muscle afferent contribution to cortical potentials. , 1988, Electroencephalography and clinical neurophysiology.

[21]  A. Schleicher,et al.  The human parietal operculum. I. Cytoarchitectonic mapping of subdivisions. , 2006, Cerebral cortex.

[22]  W. Sonntag,et al.  Age-related synaptic changes in sensorimotor cortex of the Brown Norway X Fischer 344 rat , 2000, Brain Research.

[23]  Jan Ruben,et al.  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. , 2006, Cerebral cortex.

[24]  P. Renshaw,et al.  Age-related Reduction in Functional MRI Response to Photic Stimulation , 1997, Neurology.

[25]  John A. E. Anderson,et al.  A multivariate analysis of age-related differences in default mode and task-positive networks across multiple cognitive domains. , 2010, Cerebral cortex.

[26]  D. Yousem,et al.  The effect of age on odor-stimulated functional MR imaging. , 1999, AJNR. American journal of neuroradiology.

[27]  O. Witte,et al.  Habituation within the somatosensory processing hierarchy , 2011, Behavioural Brain Research.

[28]  D. Heistad,et al.  Effects of aging on responses of cerebral arterioles. , 1990, The American journal of physiology.

[29]  H. Kugel,et al.  Age related signal decrease in functional magnetic resonance imaging during motor stimulation in humans , 2001, Neuroscience Letters.

[30]  G. Buzsáki,et al.  Inhibition and Brain Work , 2007, Neuron.

[31]  R. DeTeresa,et al.  Neocortical cell counts in normal human adult aging , 1987, Annals of neurology.

[32]  Thomas E. Nichols,et al.  Thresholding of Statistical Maps in Functional Neuroimaging Using the False Discovery Rate , 2002, NeuroImage.

[33]  M. Lindquist,et al.  Validity and power in hemodynamic response modeling: A comparison study and a new approach , 2007, Human Brain Mapping.

[34]  M. D’Esposito,et al.  The Effect of Normal Aging on the Coupling of Neural Activity to the Bold Hemodynamic Response , 1999, NeuroImage.

[35]  Hubert R. Dinse,et al.  Increased Excitability of Somatosensory Cortex in Aged Humans is Associated with Impaired Tactile Acuity , 2012, The Journal of Neuroscience.

[36]  Maurizio Corbetta,et al.  The human brain is intrinsically organized into dynamic, anticorrelated functional networks. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[37]  Patrick Ragert,et al.  Impaired tactile acuity in old age is accompanied by enlarged hand representations in somatosensory cortex. , 2009, Cerebral cortex.

[38]  J. Brunso-Bechtold,et al.  Age‐related decline of presumptive inhibitory synapses in the sensorimotor cortex as revealed by the physical disector , 2001, The Journal of comparative neurology.

[39]  Christo Pantev,et al.  Age-related changes in cortical swallowing processing , 2010, Neurobiology of Aging.

[40]  Massimiliano Valeriani,et al.  The effects of aging on selective attention to touch: a reduced inhibitory control in elderly subjects? , 2003, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[41]  Arthur F. Kramer,et al.  Dedifferentiation in the visual cortex: An fMRI investigation of individual differences in older adults , 2008, Brain Research.

[42]  E. Evans,et al.  Current perception thresholds in ageing. , 1992, Age and ageing.

[43]  Simon B. Eickhoff,et al.  A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data , 2005, NeuroImage.

[44]  W. Backes,et al.  Somatosensory cortex responses to median nerve stimulation: fMRI effects of current amplitude and selective attention , 2000, Clinical Neurophysiology.

[45]  Yong He,et al.  Aging-related changes in the default mode network and its anti-correlated networks: A resting-state fMRI study , 2011, Neuroscience Letters.

[46]  M. Erb,et al.  Relation between Regional Functional MRI Activation and Vascular Reactivity to Carbon Dioxide during Normal Aging , 2003, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[47]  D. Walsh,et al.  Transcutaneous electric nerve stimulation: the effect of intensity on local and distal cutaneous blood flow and skin temperature in healthy subjects. , 2002, Archives of physical medicine and rehabilitation.

[48]  Julia M. Stephen,et al.  Aging changes and gender differences in response to median nerve stimulation measured with MEG , 2006, Clinical Neurophysiology.

[49]  Karl J. Friston,et al.  Decreases in Regional Cerebral Blood Flow with Normal Aging , 1991, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[50]  Bradley P Sutton,et al.  Reduced somatosensory activations in swallowing with age , 2011, Human brain mapping.

[51]  R. Frackowiak,et al.  Quantitative Measurement of Regional Cerebral Blood Flow and Oxygen Metabolism in Man Using 15O and Positron Emission Tomography: Theory, Procedure, and Normal Values , 1980, Journal of computer assisted tomography.

[52]  L. Dorfman,et al.  Age‐related changes in peripheral and central nerve conduction in man , 1979, Neurology.

[53]  M F Bruce,et al.  The relation of tactile thresholds to histology in the fingers of elderly people. , 1980, Journal of neurology, neurosurgery, and psychiatry.

[54]  Robert C. Welsh,et al.  Decreased neural specialization in old adults on a working memory task , 2006, Neuroreport.

[55]  Carsten Klingner,et al.  Dependence of the negative BOLD response on somatosensory stimulus intensity , 2010, NeuroImage.

[56]  Fahmeed Hyder,et al.  Energetic basis of brain activity: implications for neuroimaging , 2004, Trends in Neurosciences.

[57]  Richard S. J. Frackowiak,et al.  Cerebral blood flow, blood volume and oxygen utilization. Normal values and effect of age. , 1990, Brain : a journal of neurology.

[58]  G. Shulman,et al.  Medial prefrontal cortex and self-referential mental activity: Relation to a default mode of brain function , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[59]  M. Lotze,et al.  Non-effective increase of fMRI-activation for motor performance in elder individuals , 2011, Behavioural Brain Research.

[60]  Otto W. Witte,et al.  Functional significance of age-related differences in motor activation patterns , 2006, NeuroImage.

[61]  H. Siebner,et al.  Age-related decrease in paired-pulse intracortical inhibition in the human primary motor cortex , 2001, Neuroscience Letters.

[62]  S. Hayasaka,et al.  Aging and the interaction of sensory cortical function and structure , 2009, Human brain mapping.

[63]  Carsten Klingner,et al.  Influences of negative BOLD responses on positive BOLD responses , 2011, NeuroImage.

[64]  O. Witte,et al.  Age-related decline of functional inhibition in rat cortex , 2010, Neurobiology of Aging.

[65]  J. Karhu,et al.  Simultaneous early processing of sensory input in human primary (SI) and secondary (SII) somatosensory cortices. , 1999, Journal of neurophysiology.

[66]  A. Leventhal,et al.  Degradation of stimulus selectivity of visual cortical cells in senescent rhesus monkeys , 2000, Nature Neuroscience.

[67]  J. Rothwell,et al.  The effect of age on task-related modulation of interhemispheric balance , 2007, Experimental Brain Research.

[68]  John C Gore,et al.  Dependence of BOLD signal change on tactile stimulus intensity in SI of primates. , 2007, Magnetic resonance imaging.

[69]  S. Folstein,et al.  "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. , 1975, Journal of psychiatric research.

[70]  Adelbert Ames,et al.  CNS energy metabolism as related to function , 2000, Brain Research Reviews.

[71]  Roberto Cabeza,et al.  Aging Gracefully: Compensatory Brain Activity in High-Performing Older Adults , 2002, NeuroImage.

[72]  C. Tseng,et al.  Aging and Current Perception Threshold Measured by Neurometer in Normal Taiwanese Adults , 2002, Journal of the American Geriatrics Society.

[73]  G Marchal,et al.  Regional cerebral oxygen consumption, blood flow, and blood volume in healthy human aging. , 1992, Archives of neurology.

[74]  E. D. Sherman,et al.  Sensitivity to Pain in the Aged. , 1960, Canadian Medical Association journal.

[75]  R. Bossemeyer,et al.  Neurological manifestations of aging. , 1977, Journal of gerontology.

[76]  Gabriel Curio,et al.  Event-related fMRI of the somatosensory system using electrical finger stimulation , 2002, Neuroreport.

[77]  G L Shulman,et al.  INAUGURAL ARTICLE by a Recently Elected Academy Member:A default mode of brain function , 2001 .