Reorganization of human motor cortex after hand replantation

In 10 patients, reorganizational changes of the motor cortex contralateral to a replanted hand (MCreplant) were studied one to 14 years after complete traumatic amputation and consecutive successful replantation of the hand. The organizational state of MCreplant was assessed for the deafferentated and peripherally deefferentated hand‐associated motor cortex and the adjacent motor representation of the proximal arm. For this, response maps were established for the first dorsal interosseus and biceps brachii muscle using focal transcranial magnetic stimulation (TMS) on a skull surface grid. Characteristics of the maps were center of gravity (COG), number of effective stimulation sites, amplitude sum, and amplitudes and response threshold at the optimal stimulation point. The COG is defined by the spatial distribution of response amplitudes on the map and lies over the cortex region with the most excitable corticospinal neurones supplying the recorded muscle. The COG of the biceps map in MCreplant was shifted laterally by 9.8 ± 3.6 mm (range 5.0–15.7 mm). The extension of the biceps map in MCreplant was increased and the responses were enlarged and had lowered thresholds. For the muscles of the replanted hand, the pattern of reorganization was different: Response amplitudes were enlarged but thresholds, COG, and area of the cortical response map were normal. The different reorganizational phenomena observed for the motor cortical areas supplying the replanted hand and the biceps brachii of the same arm may be influenced by a different extent of deafferentation and by their different role in hand motor control.

[1]  P. D. Wall,et al.  Sensory afferent impulses originate from dorsal root ganglia as well as from the periphery in normal and nerve injured rats , 1983, Pain.

[2]  J. Kaas,et al.  Large-scale sprouting of cortical connections after peripheral injury in adult macaque monkeys. , 1998, Science.

[3]  R. Töpper,et al.  Localization of the motor hand area using transcranial magnetic stimulation and functional magnetic resonance imaging , 1999, Clinical Neurophysiology.

[4]  A. Ward,et al.  Some effects of deafferentation on neurons of the cat spinal cord. , 1967, Archives of neurology.

[5]  J. Kaas,et al.  Reorganization in Primary Motor Cortex of Primates with Long-Standing Therapeutic Amputations , 1999, The Journal of Neuroscience.

[6]  J. Yokota,et al.  Divergent projection of individual corticospinal axons to motoneurons of multiple muscles in the monkey , 1981, Neuroscience Letters.

[7]  L. Cohen,et al.  Modulation of Plasticity in Human Motor Cortex after Forearm Ischemic Nerve Block , 1998, The Journal of Neuroscience.

[8]  KM Jacobs,et al.  Reshaping the cortical motor map by unmasking latent intracortical connections , 1991, Science.

[9]  B U Meyer,et al.  Long-term reorganization of motor cortex outputs after arm amputation , 1999, Neurology.

[10]  M Hallett,et al.  Physiological analysis of motor reorganization following lower limb amputation. , 1992, Electroencephalography and clinical neurophysiology.

[11]  H Piza [Transplantation of hands in Innsbruck]. , 2000, Wiener klinische Wochenschrift.

[12]  F L Mastaglia,et al.  Magnetic stimulation mapping of motor cortex: factors contributing to map area. , 1998, Electroencephalography and clinical neurophysiology.

[13]  V. Ramachandran,et al.  Synaesthesia in phantom limbs induced with mirrors , 1996, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[14]  J. Wall,et al.  Initial cortical reactions to injury of the median and radial nerves to the hands of adult primates , 1996, The Journal of comparative neurology.

[15]  V. Ramachandran,et al.  Perceptual correlates of massive cortical reorganization. , 1992, Science.

[16]  M Hallett,et al.  Mechanisms of Cortical Reorganization in Lower-Limb Amputees , 1998, The Journal of Neuroscience.

[17]  J Valls-Solé,et al.  Rapid modulation of human cortical motor outputs following ischaemic nerve block. , 1993, Brain : a journal of neurology.

[18]  C. Meuli‐Simmen,et al.  Long‐Term Follow‐Up after Finger and Upper‐Limb Replantation: Clinical, Angiologic, and Lymphographic Studies , 1998, Journal of reconstructive microsurgery.

[19]  W P Cooney,et al.  Successful hand transplantation--one year follow-up. , 2001, The New England journal of medicine.

[20]  J. Liepert,et al.  Motor plasticity induced by synchronized thumb and foot movements , 1999, Experimental Brain Research.

[21]  D J Felleman,et al.  Functional reorganization in somatosensory cortical areas 3b and 1 of adult monkeys after median nerve repair: possible relationships to sensory recovery in humans , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[22]  J. Rothwell,et al.  REORGANIZATION IN HUMAN MOTOR CORTEX , 1995 .

[23]  N. Birbaumer,et al.  Does use of a myoelectric prosthesis prevent cortical reorganization and phantom limb pain? , 1999, Nature Neuroscience.

[24]  Á. Pascual-Leone,et al.  Reorganization of human cortical motor output maps following traumatic forearm amputation , 1996, Neuroreport.

[25]  R. Schmidt,et al.  Responsiveness of the somatosensory system after nerve injury and amputation in the human hand , 1994, Annals of neurology.

[26]  Mark Hallett,et al.  Locating the Motor Cortex on the MRI with Transcranial Magnetic Stimulation and PET , 1996, NeuroImage.

[27]  Brain Aids to the Examination of the Peripheral Nervous System , 1987 .

[28]  Lars Ersland,et al.  Phantom limb imaginary fingertapping causes primary motor cortex activation: an fMRI study , 1996, Neuroreport.

[29]  T. Elbert,et al.  Phantom-limb pain as a perceptual correlate of cortical reorganization following arm amputation , 1995, Nature.

[30]  J P Malin,et al.  Cortical reorganization in patients with facial palsy , 1997, Annals of neurology.

[31]  R. Nudo,et al.  Adaptive Plasticity in Primate Motor Cortex as a Consequence of Behavioral Experience and Neuronal Injury , 1997 .

[32]  V. Ramachandran,et al.  Acute plasticity in the human somatosensory cortex following amputation , 1998, Neuroreport.

[33]  M. Hallett,et al.  Noninvasive mapping of muscle representations in human motor cortex. , 1992, Electroencephalography and clinical neurophysiology.

[34]  J G Ojemann,et al.  Cortical stimulation mapping of phantom limb rolandic cortex. Case report. , 1995, Journal of neurosurgery.

[35]  P. Schwenkreis,et al.  Changes of cortical excitability in patients with upper limb amputation , 2000, Neuroscience Letters.

[36]  M. Panizza,et al.  Modifications of the N1-P1 component of the somatosensory evoked potential in humans after partial limb amputation as a manifestation of central nervous system remodeling. , 1988, Electromyography and clinical neurophysiology.

[37]  M. Lanzettà,et al.  Human hand allograft: report on first 6 months , 1999, The Lancet.

[38]  G Zanette,et al.  Reversible changes of motor cortical outputs following immobilization of the upper limb. , 1997, Electroencephalography and clinical neurophysiology.

[39]  G Schlaug,et al.  Multimodal output mapping of human central motor representation on different spatial scales , 1998, The Journal of physiology.

[40]  M. Cynader,et al.  Somatosensory cortical map changes following digit amputation in adult monkeys , 1984, The Journal of comparative neurology.

[41]  J. Rothwell,et al.  Reorganisation in human motor cortex. , 1995, Canadian journal of physiology and pharmacology.

[42]  S. Bandinelli,et al.  Motor reorganization after upper limb amputation in man. A study with focal magnetic stimulation. , 1991, Brain : a journal of neurology.

[43]  J. Kaas,et al.  Sensory afferent projections and area 3b somatotopy following median nerve cut and repair in macaque monkeys. , 1994, Cerebral cortex.