Forces consistent with plateau-like behaviour of spinal neurons evoked in patients with spinal cord injuries.

Percutaneous electrical stimulation over tibialis anterior and triceps surae was performed in 14 patients with traumatic spinal cord injury (SCI) to look for evidence that 'extra contractions' can develop, beyond those due to activation of the motor axons beneath the stimulating electrodes. Criteria for the extra contractions included marked asymmetry of force with respect to stimulation, progressively rising force during stimulation of constant amplitude and frequency, and force remaining high after stimulation frequency had returned to the control level following a high-frequency burst. Twelve of the 14 patients showed evidence of such behaviour, more frequently in triceps surae than tibialis anterior. Force or electromyographic activity commonly outlasted the stimulation in these patients. There was no apparent correlation between the completeness or level of injury and the ability to induce the behaviour. Evidence of force potentiation and 'habituation' was also seen. Eleven of the 14 patients exhibited hyper-reflexia and reported spontaneous spasms, but there was no obvious association with the extra contractions. It is concluded that non-classical behaviour of neurons within the spinal cord can contribute to the extra contractions evoked by electrical stimulation over muscles in spinal cord-injured subjects. This central contribution is less easy to obtain than in intact healthy subjects, all of whom showed the phenomenon. These contractions are consistent with the activation of plateau potentials in spinal neurons and, if so, plateau potentials may contribute to a patient's clinical manifestations.

[1]  C. G. Phillips,et al.  Differentiation of tonic from phasic alpha ventral horn cells by stretch, pinna and crossed extensor reflexes. , 1957, Journal of neurophysiology.

[2]  D. Kernell.  The Adaptation and the Relation between Discharge Frequency and Current Strength of Cat Lumbosacral Motoneurones Stimulated by Long‐Lasting Injected Currents , 1965 .

[3]  R. Granit.  Muscular Afferents and Motor Control , 1966 .

[4]  G. Eklund,et al.  Normal variability of tonic vibration reflexes in man. , 1966, Experimental neurology.

[5]  D. Kernell,et al.  Algebraical summation in synaptic activation of motoneurones firing within the ‘primary range’ to injected currents , 1966, The Journal of physiology.

[6]  J. Lance,et al.  Differential effects on tonic and phasic reflex mechanisms produced by vibration of muscles in man. , 1966, Journal of neurology, neurosurgery, and psychiatry.

[7]  M. Dimitrijevic,et al.  Studies of spasticity in man. I. Some features of spasticity. , 1967, Brain : a journal of neurology.

[8]  A. Lang,et al.  Motoneuron activation by low intensity tetanic stimulation of muscle afferents in man. , 1967, Experimental neurology.

[9]  Muscular afferents and motor control. By Ragner Granit (ed.) John Wiley Sons, Inc., New York, N. Y. 1966. 466 pp. $20.00 , 1967 .

[10]  G. Eklund,et al.  The effects of muscle vibration in spasticity, rigidity, and cerebellar disorders. , 1968, Journal of neurology, neurosurgery, and psychiatry.

[11]  M. Dimitrijevic,et al.  Studies of spasticity in man. 3. Analysis of revlex activity evoked by noxious cutaneous stimulation. , 1968, Brain : a journal of neurology.

[12]  M. Dimitrijevic,et al.  Studies of spasticity in man. 4. Changes in flexion reflex with repetitive cutaneous stimulation in spinal man. , 1970, Brain : a journal of neurology.

[13]  R R Young,et al.  Human flexor reflexes , 1971, Journal of neurology, neurosurgery, and psychiatry.

[14]  D. Burke,et al.  Tonic vibration reflex in spasticity, Parkinson's disease, and normal subjects , 1972, Journal of neurology, neurosurgery, and psychiatry.

[15]  H. Wigström,et al.  Prolonged activation of soleus motoneurones following a conditioning train in soleus Ia afferents — A case for a reverberating loop? , 1975, Neuroscience Letters.

[16]  D. H. Paul.  The physiology of nerve cells , 1975 .

[17]  P. Schwindt,et al.  Role of a persistent inward current in motoneuron bursting during spinal seizures. , 1980, Journal of neurophysiology.

[18]  O. Kiehn,et al.  Transmitter-controlled properties of alpha-motoneurones causing long-lasting motor discharge to brief excitatory inputs. , 1986, Progress in brain research.

[19]  Y. Nakajima,et al.  Long-lasting afterdischarge of alpha-motoneurons after muscle vibration or electrical stimulation of Group I afferent fibers in the anemically decerebrated cat , 1989, Neuroscience Research.

[20]  O Kiehn,et al.  Bistable firing properties of soleus motor units in unrestrained rats. , 1989, Acta physiologica Scandinavica.

[21]  D. Burke,et al.  Task‐dependent changes in the responses to low‐threshold cutaneous afferent volleys in the human lower limb. , 1991, The Journal of physiology.

[22]  D. McCrea.  Can sense be made of spinal interneuron circuits , 1992 .

[23]  Ole Kiehn,et al.  Neuromodulation of vertebrate motor neuron membrane properties , 1992, Current Opinion in Neurobiology.

[24]  R. Quencer,et al.  Observations on the pathology of human spinal cord injury. A review and classification of 22 new cases with details from a case of chronic cord compression with extensive focal demyelination. , 1993, Advances in neurology.

[25]  Randall K. Powers,et al.  How different afferent inputs control motoneuron discharge and the output of the motoneuron pool , 1993, Current Opinion in Neurobiology.

[26]  P. Cavallari,et al.  Motor neuron 'bistability'. A pathogenetic mechanism for cramps and myokymia. , 1994, Brain : a journal of neurology.

[27]  B Decchi,et al.  Flexibility of lower limb reflex responses to painful cutaneous stimulation in standing humans: evidence of load‐dependent modulation. , 1994, The Journal of physiology.

[28]  Upper extremity neuropathies in patients with spinal cord injuries. , 1995, The journal of spinal cord medicine.

[29]  D. D. Fraser,et al.  Cholinergic-Dependent Plateau Potential in Hippocampal CA1 Pyramidal Neurons , 1996, The Journal of Neuroscience.

[30]  O. Kiehn,et al.  Prolonged firing in motor units: evidence of plateau potentials in human motoneurons? , 1997, Journal of neurophysiology.

[31]  Jaynie F. Yang,et al.  Self-sustained firing of human motor units , 1998, Neuroscience Letters.

[32]  C. Heckman,et al.  Bistability in spinal motoneurons in vivo: systematic variations in rhythmic firing patterns. , 1998, Journal of neurophysiology.

[33]  H Hultborn,et al.  Synaptic activation of plateaus in hindlimb motoneurons of decerebrate cats. , 1998, Journal of neurophysiology.

[34]  H Hultborn,et al.  Short-term plasticity in hindlimb motoneurons of decerebrate cats. , 1998, Journal of neurophysiology.

[35]  Robert H. Lee,et al.  The role of voltage-sensitive dendritic conductances in generating bistable firing patterns in motoneurons , 1999, Journal of Physiology-Paris.

[36]  M. Gorassini,et al.  Activation patterns of hindlimb motor units in the awake rat and their relation to motoneuron intrinsic properties. , 1999, Journal of neurophysiology.

[37]  A Curt,et al.  Diagnostic and prognostic value of compound motor action potential of lower limbs in acute paraplegic patients , 2000, Spinal Cord.

[38]  J. Hounsgaard,et al.  Development and regulation of response properties in spinal cord motoneurons , 2000, Brain Research Bulletin.

[39]  C. Heckman,et al.  Adjustable Amplification of Synaptic Input in the Dendrites of Spinal Motoneurons In Vivo , 2000, The Journal of Neuroscience.

[40]  J. Lopez-Garcia,et al.  Wind-up of spinal cord neurones and pain sensation: much ado about something? , 2000, Progress in Neurobiology.

[41]  R. Harris-Warrick,et al.  Contributions of intrinsic motor neuron properties to the production of rhythmic motor output in the mammalian spinal cord , 2000, Brain Research Bulletin.

[42]  W. Rymer,et al.  Flexor reflexes in chronic spinal cord injury triggered by imposed ankle rotation , 2000, Muscle & nerve.

[43]  S C Gandevia,et al.  Large Involuntary Forces Consistent with Plateau-Like Behavior of Human Motoneurons , 2001, The Journal of Neuroscience.

[44]  M. Gorassini,et al.  Evidence for plateau potentials in tail motoneurons of awake chronic spinal rats with spasticity. , 2001, Journal of neurophysiology.

[45]  M. Siu,et al.  Plateau potentials in sacrocaudal motoneurons of chronic spinal rats, recorded in vitro. , 2001, Journal of neurophysiology.

[46]  D. Burke,et al.  Sustained contractions produced by plateau‐like behaviour in human motoneurones , 2002, The Journal of physiology.

[47]  Jaynie F. Yang,et al.  Intrinsic activation of human motoneurons: possible contribution to motor unit excitation. , 2002, Journal of neurophysiology.

[48]  T George Hornby,et al.  Motoneurons: A preferred firing range across vertebrate species? , 2002, Muscle & nerve.

[49]  J. Hounsgaard.  Motoneurons do what motoneurons have to do , 2002, The Journal of physiology.

[50]  Bruno Delord,et al.  A biophysical model of nonlinear dynamics underlying plateau potentials and calcium spikes in purkinje cell dendrites. , 2002, Journal of neurophysiology.

[51]  Inge Zijdewind,et al.  Motor unit firing during and after voluntary contractions of human thenar muscles weakened by spinal cord injury. , 2003, Journal of neurophysiology.

[52]  M. Akai,et al.  Sustained muscle contractions maintained by autonomous neuronal activity within the human spinal cord. , 2003, Journal of neurophysiology.

[53]  W. Rymer,et al.  Windup of flexion reflexes in chronic human spinal cord injury: a marker for neuronal plateau potentials? , 2003, Journal of neurophysiology.

[54]  Hans Hultborn,et al.  Variable amplification of synaptic excitation and inhibition in spinal motoneurones by dendritic persistent inward current. , 2003 .

[55]  L. M. Jordan,et al.  On the regulation of repetitive firing in lumbar motoneurones during fictive locomotion in the cat , 1992, Experimental Brain Research.