Paired associative stimulation induces change in presynaptic inhibition of Ia terminals in wrist flexors in humans.

Enhancements in the strength of corticospinal projections to muscles are induced in conscious humans by paired associative stimulation (PAS) to the motor cortex. Although most of the previous studies support the hypothesis that the increase of the amplitude of motor evoked potentials (MEPs) by PAS involves long-term potentiation (LTP)-like mechanism in cortical synapses, changes in spinal excitability after PAS have been reported, suggestive of parallel modifications in both cortical and spinal excitability. In a first series of experiments (experiment 1), we confirmed that both flexor carpi radialis (FCR) MEPs and FCR H reflex recruitment curves are enhanced by PAS. To elucidate the mechanism responsible for this change in the H reflex amplitude, we tested, using the same subjects, the hypothesis that enhanced H reflexes are caused by a down-regulation of the efficacy of mechanisms controlling Ia afferent discharge, including presynaptic Ia inhibition and postactivation depression. To address this question, amounts of both presynaptic Ia inhibition of FCR Ia terminals (D1 and D2 inhibitions methods; experiment 2) and postactivation depression (experiment 3) were determined before and after PAS. Results showed that PAS induces a significant decrease of presynaptic Ia inhibition of FCR terminals, which was concomitant with the facilitation of the H reflex. Postactivation depression was unaffected by PAS. It is argued that enhancement of segmental excitation by PAS relies on a selective effect of PAS on the interneurons controlling presynaptic inhibition of Ia terminals.

[1]  V Achache,et al.  Impact of transcranial direct current stimulation on spinal network excitability in humans , 2009, The Journal of physiology.

[2]  A. Oliviero,et al.  Associative motor cortex plasticity: direct evidence in humans. , 2009, Cerebral cortex.

[3]  M. Hallett,et al.  Associative plasticity in intracortical inhibitory circuits in human motor cortex , 2009, Clinical Neurophysiology.

[4]  J. Rothwell,et al.  The effect of continuous theta burst stimulation over premotor cortex on circuits in primary motor cortex and spinal cord , 2009, Clinical Neurophysiology.

[5]  A. Oliviero,et al.  LTD-like plasticity induced by paired associative stimulation: direct evidence in humans , 2009, Experimental Brain Research.

[6]  R. Katz,et al.  Impaired efficacy of spinal presynaptic mechanisms in spastic stroke patients. , 2009, Brain : a journal of neurology.

[7]  Jens Bo Nielsen,et al.  Central nervous adaptations following 1 wk of wrist and hand immobilization. , 2008, Journal of applied physiology.

[8]  J. Rothwell,et al.  Consensus: Motor cortex plasticity protocols , 2008, Brain Stimulation.

[9]  E. Paul Zehr,et al.  A sigmoid function is the best fit for the ascending limb of the Hoffmann reflex recruitment curve , 2008, Experimental Brain Research.

[10]  M. Gorassini,et al.  Role of sustained excitability of the leg motor cortex after transcranial magnetic stimulation in associative plasticity. , 2007, Journal of neurophysiology.

[11]  M. Hallett,et al.  Changes in spinal excitability after PAS. , 2007, Journal of neurophysiology.

[12]  S. Meunier,et al.  Impaired modulation of motor cortex excitability by homonymous and heteronymous muscle afferents in focal hand dystonia , 2007, Movement disorders : official journal of the Movement Disorder Society.

[13]  T Sinkjaer,et al.  Changes in excitability of the cortical projections to the human tibialis anterior after paired associative stimulation. , 2007, Journal of neurophysiology.

[14]  K. Stefan,et al.  The two sides of associative plasticity in writer's cramp. , 2006, Brain : a journal of neurology.

[15]  T. Bliss,et al.  Plasticity in the human central nervous system. , 2006, Brain : a journal of neurology.

[16]  J. Wolpaw,et al.  Plasticity from muscle to brain , 2006, Progress in Neurobiology.

[17]  David Burke,et al.  The Circuitry of the Human Spinal Cord: Its Role in Motor Control and Movement Disorders , 2005 .

[18]  A. Pénicaud,et al.  Post-activation depression in various group I spinal pathways in humans , 2005, Experimental Brain Research.

[19]  J. Nielsen,et al.  Short-term adaptations in spinal cord circuits evoked by repetitive transcranial magnetic stimulation: possible underlying mechanisms , 2005, Experimental Brain Research.

[20]  W D Byblow,et al.  Excitability changes in human forearm corticospinal projections and spinal reflex pathways during rhythmic voluntary movement of the opposite limb , 2004, The Journal of physiology.

[21]  K. Stefan,et al.  Modulation of associative human motor cortical plasticity by attention. , 2004, Journal of neurophysiology.

[22]  S C Gandevia,et al.  Noninvasive stimulation of the human corticospinal tract. , 2004, Journal of applied physiology.

[23]  J. Rothwell,et al.  One‐Hz repetitive transcranial magnetic stimulation of the premotor cortex alters reciprocal inhibition in DYT1 dystonia , 2004, Movement disorders : official journal of the Movement Disorder Society.

[24]  T. Hortobágyi,et al.  Changes in segmental and motor cortical output with contralateral muscle contractions and altered sensory inputs in humans. , 2003, Journal of neurophysiology.

[25]  L. Cohen,et al.  A temporally asymmetric Hebbian rule governing plasticity in the human motor cortex. , 2003, Journal of neurophysiology.

[26]  J. Nielsen,et al.  Interaction between peripheral afferent activity and presynaptic inhibition of ia afferents in the cat. , 2002, Journal of neurophysiology.

[27]  Stephan Riek,et al.  The sites of neural adaptation induced by resistance training in humans , 2002, The Journal of physiology.

[28]  L. Cohen,et al.  Mechanisms of enhancement of human motor cortex excitability induced by interventional paired associative stimulation , 2002, The Journal of physiology.

[29]  J. Rothwell,et al.  Are the after-effects of low-frequency rTMS on motor cortex excitability due to changes in the efficacy of cortical synapses? , 2001, Clinical Neurophysiology.

[30]  S. Schultz.  Principles of Neural Science, 4th ed. , 2001 .

[31]  A. Pénicaud,et al.  Modulation of presynaptic inhibition of Ia afferents during voluntary wrist flexion and extension in man , 2001, Experimental Brain Research.

[32]  L. Cohen,et al.  Enhancing the quality of studies using transcranial magnetic and electrical stimulation with a new computer-controlled system , 2000, Journal of Neuroscience Methods.

[33]  D. Mazevet,et al.  The monosynaptic reflex: a tool to investigate motor control in humans. Interest and limits , 2000, Neurophysiologie Clinique/Clinical Neurophysiology.

[34]  L. Cohen,et al.  Induction of plasticity in the human motor cortex by paired associative stimulation. , 2000, Brain : a journal of neurology.

[35]  R. Schmidt,et al.  Presynaptic inhibition in the vertebrate spinal cord revisited , 1999, Experimental Brain Research.

[36]  J. Rothwell,et al.  Inhibitory action of forearm flexor muscle afferents on corticospinal outputs to antagonist muscles in humans , 1998, The Journal of physiology.

[37]  S. Meunier,et al.  Cortical control of presynaptic inhibition of Ia afferents in humans , 1998, Experimental Brain Research.

[38]  Jonathan R. Wolpaw,et al.  The complex structure of a simple memory , 1997, Trends in Neurosciences.

[39]  M. Hallett,et al.  Depression of motor cortex excitability by low‐frequency transcranial magnetic stimulation , 1997, Neurology.

[40]  M. Illert,et al.  On the mechanism of the post-activation depression of the H-reflex in human subjects , 1996, Experimental Brain Research.

[41]  P. Rossini,et al.  Non-invasive electrical and magnetic stimulation of the brain, spinal cord and roots: basic principles and procedures for routine clinical application. Report of an IFCN committee. , 1994, Electroencephalography and clinical neurophysiology.

[42]  M D Binder,et al.  Computer simulations of the effects of different synaptic input systems on motor unit recruitment. , 1993, Journal of neurophysiology.

[43]  A. Lev-Tov,et al.  In vitro studies of prolonged synaptic depression in the neonatal rat spinal cord. , 1992, The Journal of physiology.

[44]  B. Day,et al.  Evidence favouring presynaptic inhibition between antagonist muscle afferents in the human forearm. , 1987, The Journal of physiology.

[45]  M. Davies,et al.  The effects of benzodiazepines on spinal homosynaptic depression , 1985, Neuropharmacology.

[46]  C. Marsden,et al.  Reciprocal inhibition between the muscles of the human forearm. , 1984, The Journal of physiology.

[47]  M. Alexander,et al.  Principles of Neural Science , 1981 .

[48]  R. Tanaka,et al.  Reciprocal group I inhibition on triceps surae motoneurons in man. , 1971, Journal of neurophysiology.

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

[50]  A. Lundberg,et al.  The effect of DOPA on the spinal cord. 1. Influence on transmission from primary afferents. , 1966, Acta physiologica Scandinavica.

[51]  G. Somjen,et al.  Excitability and inhibitability of motoneurons of different sizes. , 1965, Journal of neurophysiology.

[52]  J. Knott.  The organization of behavior: A neuropsychological theory , 1951 .

[53]  U. Ziemann.  LTP-like plasticity in human motor cortex. , 2004, Supplements to Clinical neurophysiology.

[54]  J. Nielsen,et al.  Methodological implications of the post activation depression of the soleus H-reflex in man , 2004, Experimental Brain Research.

[55]  J. Wolpaw,et al.  Activity-dependent spinal cord plasticity in health and disease. , 2001, Annual review of neuroscience.

[56]  J. Wolpaw,et al.  Operant conditioning of rat H-reflex affects motoneuron axonal conduction velocity , 2000, Experimental Brain Research.

[57]  C. Crone,et al.  Amplitude of the maximum motor response (Mmax) in human muscles typically decreases during the course of an experiment , 1999, Experimental Brain Research.

[58]  J C Rothwell,et al.  Physiological studies of electric and magnetic stimulation of the human brain. , 1991, Electroencephalography and clinical neurophysiology. Supplement.

[59]  D. O. Hebb,et al.  The organization of behavior , 1988 .

[60]  K. Frank.  Presynaptic and postsynaptic inhibition of monosynaptic reflexes , 1957 .