Age-Related Changes in Motor Cortical Representation and Interhemispheric Interactions: A Transcranial Magnetic Stimulation Study

To better understand the physiological mechanisms responsible for the differential motor cortex functioning in aging, we used transcranial magnetic stimulation to investigate interhemispheric interactions and cortical representation of hand muscles in the early phase of physiological aging, correlating these data with participants’ motor abilities. Right-handed healthy subjects were divided into a younger group (n = 15, mean age 25.4 ± 1.9 years old) and an older group (n = 16, mean age 61.1 ± 5.1 years old). Activity of the bilateral abductor pollicis brevis (APB) and abductor digiti minimi (ADM) was recorded. Ipsilateral silent period (ISP) was measured in both APBs. Cortical maps of APB and ADM were measured bilaterally. Mirror movements (MM) were recorded during thumb abductions. Motor abilities were tested using Nine Hole Peg Test, finger tapping, and grip strength. ISP was reduced in the older group on both sides, in terms of duration (p = 0.025), onset (p = 0.029), and area (p = 0.008). Resting motor threshold did not differ between groups. APB and ADM maps were symmetrical in the younger group, but were reduced on the right compared to the left hemisphere in the older group (p = 0.008). The APB map of the right hemisphere was reduced in the older group compared to the younger (p = 0.021). Older subjects showed higher frequency of MM and worse motor abilities (p < 0.001). The reduction of right ISP area correlated significantly with the worsening of motor performances. Our results showed decreased interhemispheric interactions in the early processes of physiological aging and decreased cortical muscles representation over the non-dominant hemisphere. The decreased ISP and increased frequency of MM suggest a reduction of transcallosal inhibition. These data demonstrate that early processes of normal aging are marked by a dissociation of motor cortices, characterized, at least, by a decline of the non-dominant hemisphere, reinforcing the hypothesis of the right hemi-aging model.

[1]  Charles J. Wysocki,et al.  Hand preference and age in the United States , 1992, Neuropsychologia.

[2]  Laura Avanzino,et al.  Suppression of the transcallosal motor output: a transcranial magnetic stimulation study in healthy subjects , 2004, Experimental Brain Research.

[3]  T. Miles,et al.  Age and sex differences in human motor cortex input–output characteristics , 2003, The Journal of physiology.

[4]  L. Leocani,et al.  Interhemispheric Balance in Parkinson's Disease: A Transcranial Magnetic Stimulation Study , 2013, Brain Stimulation.

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

[6]  Takayuki Obata,et al.  Age-related degeneration of corpus callosum measured with diffusion tensor imaging , 2006, NeuroImage.

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

[8]  Kimatha Oxford Grice,et al.  Adult norms for a commercially available Nine Hole Peg Test for finger dexterity. , 2003, The American journal of occupational therapy : official publication of the American Occupational Therapy Association.

[9]  N. De Stefano,et al.  Age-related changes in conventional, magnetization transfer, and diffusion-tensor MR imaging findings: study with whole-brain tissue histogram analysis. , 2003, Radiology.

[10]  T. Davidson,et al.  Age and hemispheric differences in transcallosal inhibition between motor cortices: an ispsilateral silent period study , 2013, BMC Neuroscience.

[11]  P. Derambure,et al.  Oscillatory cortical activity related to voluntary muscle relaxation: Influence of normal aging , 2006, Clinical Neurophysiology.

[12]  T J Doherty,et al.  Effects of ageing on the motor unit: a brief review. , 1993, Canadian journal of applied physiology = Revue canadienne de physiologie appliquee.

[13]  L. Leocani,et al.  Cortical control of unilateral simple movement in healthy aging , 2011, Neurobiology of Aging.

[14]  Lucien T. Thompson,et al.  Calcium-dependent afterhyperpolarization and learning in young and aging hippocampus. , 1996, Life sciences.

[15]  K. Lim,et al.  Age‐related decline in brain white matter anisotropy measured with spatially corrected echo‐planar diffusion tensor imaging , 2000, Magnetic resonance in medicine.

[16]  S. Rossi,et al.  Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research , 2009, Clinical Neurophysiology.

[17]  Traian Popa,et al.  Congenital mirror movements: a clue to understanding bimanual motor control , 2011, Journal of Neurology.

[18]  P. M. Rossini,et al.  Age-related changes of motor evoked potentials in healthy humans: Non-invasive evaluation of central and peripheral motor tracts excitability and conductivity , 1992, Brain Research.

[19]  C. Gerloff,et al.  The influence of normal aging on the cortical processing of a simple motor task , 2000, Neurology.

[20]  M. Cincotta,et al.  Mirror Movements in Movement Disorders: A Review , 2012, Tremor and other hyperkinetic movements.

[21]  M. Cincotta,et al.  Neurophysiology of unimanual motor control and mirror movements , 2008, Clinical Neurophysiology.

[22]  John L. Bradshaw,et al.  Investigating the cortical origins of motor overflow , 2004, Brain Research Reviews.

[23]  J. Callicott,et al.  Neurophysiological correlates of age-related changes in human motor function , 2002, Neurology.

[24]  Elisabetta Coppi,et al.  Mapping Early Changes of Cortical Motor Output after Subcortical Stroke: A Transcranial Magnetic Stimulation Study , 2013, Brain Stimulation.

[25]  Michael Alexander,et al.  Age-Related Differences in Movement Representation , 2002, NeuroImage.

[26]  M. Petitjean,et al.  An age-related change in the ipsilateral silent period of a small hand muscle , 2011, Clinical Neurophysiology.

[27]  A. Pfefferbaum,et al.  Increased brain white matter diffusivity in normal adult aging: Relationship to anisotropy and partial voluming , 2003, Magnetic resonance in medicine.

[28]  Heidi Johansen-Berg,et al.  Functional anatomy of interhemispheric cortical connections in the human brain , 2006, Journal of anatomy.

[29]  D. Irving,et al.  The numbers of limb motor neurons in the human lumbosacral cord throughout life , 1977, Journal of the Neurological Sciences.

[30]  B. Steinhoff,et al.  Effects of antiepileptic drugs on motor cortex excitability in humans: A transcranial magnetic stimulation study , 1996, Annals of neurology.

[31]  Steven C Cramer,et al.  Age and Features of Movement Influence Motor Overflow , 2003, Journal of the American Geriatrics Society.

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

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

[34]  T. A. Pitler,et al.  Prolonged Ca2+-dependent afterhyperpolarizations in hippocampal neurons of aged rats. , 1984, Science.

[35]  Christophe Tandonnet,et al.  Age-related Differences in Corticomotor Excitability and Inhibitory Processes during a Visuomotor RT Task , 2012, Journal of Cognitive Neuroscience.

[36]  N. Ward,et al.  Age-dependent changes in the neural correlates of force modulation: An fMRI study , 2008, Neurobiology of Aging.

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

[38]  D. Head,et al.  Differential vulnerability of anterior white matter in nondemented aging with minimal acceleration in dementia of the Alzheimer type: evidence from diffusion tensor imaging. , 2004, Cerebral cortex.

[39]  G. Akopian,et al.  Pre‐ and postsynaptic contributions to age‐related alterations in corticostriatal synaptic plasticity , 2006, Synapse.

[40]  J. Stephens,et al.  A neurophysiological study of mirror movements in adults and children , 1999, Annals of neurology.

[41]  Antonino Vallesi,et al.  Age effects on the asymmetry of the motor system: Evidence from cortical oscillatory activity , 2010, Biological Psychology.

[42]  R L Iman,et al.  Analysis of covariance using the rank transformation. , 1982, Biometrics.

[43]  B. Meyer,et al.  Inhibitory and excitatory interhemispheric transfers between motor cortical areas in normal humans and patients with abnormalities of the corpus callosum. , 1995, Brain : a journal of neurology.

[44]  Ulf Ziemann,et al.  Modulation of interhemispheric inhibition by volitional motor activity: an ipsilateral silent period study , 2009, The Journal of physiology.

[45]  Haruyasu Yamada,et al.  Normal aging in the central nervous system: quantitative MR diffusion-tensor analysis , 2002, Neurobiology of Aging.

[46]  R. Cabeza,et al.  Hemispheric asymmetry and aging: right hemisphere decline or asymmetry reduction , 2002, Neuroscience & Biobehavioral Reviews.

[47]  R. C. Oldfield.  The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[48]  P. A. Tonali,et al.  Effects of aging on motor cortex excitability , 2006, Neuroscience Research.

[49]  M. Kiernan,et al.  Cortical excitability differences in hand muscles follow a split‐hand pattern in healthy controls , 2014, Muscle & nerve.

[50]  Philip W. Landfield,et al.  Elevated Postsynaptic [Ca2+]iand L-Type Calcium Channel Activity in Aged Hippocampal Neurons: Relationship to Impaired Synaptic Plasticity , 2001, The Journal of Neuroscience.

[51]  Robert Chen,et al.  Organization of ipsilateral excitatory and inhibitory pathways in the human motor cortex. , 2003, Journal of neurophysiology.