Changes of medium-latency SEP-components following peripheral nerve lesion^[*]

Abstract

Background Animal studies have demonstrated complex cortical reorganization following peripheral nerve lesion. Central projection fields of intact nerves supplying skin areas which border denervated skin, extended into the deafferentiated cortical representation area. As a consequence of nerve lesions and subsequent reorganization an increase of the somatosensory evoked potentials (SEPs) was observed in cats when intact neighbouring nerves were stimulated. An increase of SEP-components of patients with nerve lesions may indicate a similar process of posttraumatic plastic cortical reorganization.

Methods To test if a similar process of post-traumatic plastic cortical reorganization does occur in humans, the SEP of intact neighbouring hand nerves were recorded in 29 patients with hand nerve lesions. To hypothetically explain the observed changes of SEP-components, SEP recording following paired stimulation of the median nerve was performed in 12 healthy subjects.

Results Surprisingly 16 of the 29 patients (55.2%) showed a reduction or elimination of N35, P45 and N60. Patients with lesions of two nerves showed more SEP-changes than patients with a single nerve lesion (85.7%; 6/7 nerves; vs. 34.2%; 13/38 nerves; Fisher’s exact test, p < 0.05). With paired stimulation a suppression of the amplitude of N20, P25 and P45 (p < 0.05; sign test), and a marked increment of N35 (p < 0.05; sign test) and N60 (not significant; sign test) of the second response could be observed.

Conclusion The results of the present investigation do not provide evidence of collateral innervation of peripherally denervated cortical neurons by neurons of adjacent cortical representation areas. They rather suggest that secondary components of the excitatory response to nerve stimulation are lost in cortical areas, which surround the denervated region.

^*This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

• References

• 1 Franck JI. Functional reorganization of cat somatic sensory-motor cortex (SmI) after selective dorsal root rhizotomies. Brain Res 1980; 186: 458-462 10.1016/0006-8993(80)90991-9 7357463
• 2 Garraghty PE, Kaas JH. Large-scale functional reorganization in adult monkey cortex after peripheral nerve injury. Proc Natl Acad Sci USA 1991; 88: 6976-6980 52216 1871112 10.1073/pnas.88.16.6976
• 3 Kaas JH, Merzenich MM, Killackey HP. The reorganization of somatosensory cortex following peripheral nerve damage in adult and developing mammals. Ann Rev Neurosci 1983; 6: 325-356 10.1146/annurev.ne.06.030183.001545 6340591
• 4 Kawakami Y, Suzuki H, Dong WK. Assessment of peripheral nerve crush injury with cortical somatosensory evoked potentials in the cat. Exp Neurol 1989; 103: 146-153 10.1016/0014-4886(89)90075-7 2912757
• 5 Kelahan AM, Ray RH, Carson LV, Massey CE. Functional reorganization of adult raccoon somatosensory cerebral cortex following neonatal digit amputation. Brain Res 1981; 223: 151-159 10.1016/0006-8993(81)90815-5
• 6 Merzenich MM, Kaas JH, Wall JT, Sur M, Nelson RJ. Progression of change following median nerve section in the cortical representation of the hand in areas 3b and 1 in adult owl and squirrel monkeys. Neuroscience 1983; 10 (3) 639-665 10.1016/0306-4522(83)90208-7 6646426
• 7 Merzenich MM, Jenkins WM. Reorganization of cortical representations of the hand following alterations of skin inputs induced by nerve injury, skin island transfers, and experience.. J Hand Ther 1993; 6 (2) 89-104 8393727
• 8 Pons TP, Garraghty PE, Ommaya AK, Kaas JH, Taub E, Mishkin M. Massive cortical reorganization after sensory deafferentation in adult macaques. Science 1991; 252: 1857-1859 10.1126/science.1843843 1843843
• 9 Jasper HH. The ten twenty electrode system of the international federation. Electroencephalogr Clin Neurophysiol 1958; 10: 371-375
• 10 Steriade M, Deschenes M. Cortical interneurons during sleep and waking in freely moving primates. Brain Res 1973; 50 (1) 192-199 10.1016/0006-8993(73)90608-2 4347845
• 11 Purpura DP, Shofer RJ. Cortical Intracellular Potentials During Augmenting and Recruiting Responses. I. Effects of Injected Hyperpolarizing Currents on Evoked Membrane Potential Changes. J Neurophysiol 1964; 27: 117-132 14132492
• 12 Creutzfeldt OD, Watanabe S, Lux HD. Relations between EEG phenomena and potentials of single cortical cells. I. Evoked responses after thalamic and erpicortical stimulation. Electroencephalogr Clin Neurophysiol 1966; 20 (1) 1-18 10.1016/0013-4694(66)90136-2 4161317
• 13 Morin D, Steriade M. Development from primary to augmenting responses in the somatosensory system. Brain Res 1981; 205 (1) 49-66 10.1016/0006-8993(81)90719-8 6258710
• 14 Castro-Alamancos MA. The augmenting response, a form of short-term plasticity in the neocortex that is modulated by behavioral state. Mol Psychiatry 1996; 1 (6) 424-426 9154239
• 15 Castro-Alamancos MA, Connors BW. Cellular mechanisms of the augmenting response: short-term plasticity in a thalamocortical pathway. J Neurosci 1996; 16 (23) 7742-7756 8922430
• 16 Metherate R, Ashe JH. Facilitation of an NMDA receptor-mediated EPSP by paired-pulse stimulation in rat neocortex via depression of GABAergic IPSPs. J Physiol 1994; 481 ( Pt 2): 331-348 1155933 7738829
• 17 Nunez A, Amzica F, Steriade M. Electrophysiology of cat association cortical cells in vivo: intrinsic properties and synaptic responses. J Neurophysiol 1993; 70 (1) 418-430 8395586
• 18 Gardner EP, Hamalainen HA, Warren S, Davis J, Young W. Somatosensory evoked potentials (SEPs) and cortical single unit responses elicited by mechanical tactile stimuli in awake monkeys. Electroencephalogr Clin Neurophysiol 1984; 58 (6) 537-552 10.1016/0013-4694(84)90044-0 6209104
• 19 Sasaki K, Staunton HP, Dieckmann G. Characteristic features of augmenting and recruiting responses in the cerebral cortex. Exp Neurol 1970; 26 (2) 369-392 10.1016/0014-4886(70)90133-0 4313184
• 20 Morison RS, Dempsey EW. Mechanism of thalamocortical augmentation and repetition.. Am J Physiol 1943; 138: 297-308
• 21 Landry P, Deschenes M. Intracortical arborizations and receptive fields of identified ventrobasal thalamocortical afferents to the primary somatic sensory cortex in the cat. J Comp Neurol 1981; 199 (3) 345-371 10.1002/cne.901990304 7263953