Functional role of plateau potentials in vertebrate motor neurons

Current Opinion in Neurobiology

Volumn 8, Issue 6, 1998, Pages 746-752

  Kiehn, Ole ^a   Eken, Torsten ^b  

^a Section of Neurophysiology   (Denmark)

^b UNIVERSITY OF OSLO   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

ACTION POTENTIAL; HUMAN; MOTONEURON; MOTOR CONTROL; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; RAT; REVIEW; SPINAL CORD;

EID: 0031696274     PISSN: 09594388     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-4388(98)80117-7     Document Type: Article

References (39)

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8. Hounsgaard J, Kiehn O. Serotonin-induced bistability of turtle motoneurones caused by a nifedipine-sensitive calcium plateau potential. J Physiol. 414:1989;265-282.
9. A receptor activation suppresses the generation of plateau potentials by decreasing the L-like calcium current and increasing the input conductance. These results show that multiple transmitters control the expression of plateau potentials in turtle motor neurons and that the effects are mediated through the modulation of several conductances.
10. 1A, mGlu1, and muscarine receptors. These findings demonstrate that natural release of transmitters from descending fiber systems can promote plateau properties through metabotropic receptor activation.
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16. Kiehn O, Harris-Warrick RM. 5-HT modulation of hyperpolarization-activated inward current and calcium-dependent outward current in a crustacean motor neuron. J Neurophysiol. 68:1992;496-508.
17. Zhang B, Harris-Warrick RM. Calcium-dependent plateau potentials in a crab stomatogastric ganglion motor neuron. I. Calcium current and its modulation by serotonin. J Neurophysiol. 74:1995;1929-1937.
18. K(Ca) did not elicit robust membrane bistability in TMNs, the authors propose that 5-HT, in addition to reducing outward currents, enhances inward current(s), in particular the L-like calcium current.
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20. CAN) present in many invertebrate and vertebrate neurons. While many CAN channels are voltage insensitive, the calcium-activated plateau current in ambiguus neurons is very sensitive to voltage.
21. 1 agonist. Under those conditions, 35% of the recorded cells produced steady firing, out-lasting the stimulus for more than 3 s. This group of cells was classified as 'fully bistable', and probably innervates fatigue-resistant muscle fibers. 65% of the motor neurons produced prolonged firing lasting less than 3 s. This group of cells was classified as 'partially bistable' and probably innervates fast-fatigable muscle fibers. The 'fully bistable' motor neurons displayed a jump in firing frequency immediately upon initiation of rhythmic firing, while a similar frequency jump in 'partially bistable' motor neurons appeared later after recruitment. The relationship between the persistent inward plateau current and the firing characteristic of 'fully bistable' and 'partially bistable' neurons was investigated in an accompanying paper [22]. Both types of cells displayed a region of negative slope conductance region in the steady state I - V relationship. The activation and deactivation of the inward plateau current occurred at a significantly more hyperpolarized level in 'fully bistable' cells than in 'partially bistable' cells. Thus, the onset threshold for the plateau current in 'fully bistable' motor neurons was close to or below the action potential threshold, while it was above the threshold for action potential generation in 'partially bistable' motor neurons. These fundamentally different types of I - V relationships are schematically illustrated in Figure 1 of this review (Figure 1 aii and bii) and may serve to explain the difference in firing behavior between motor neurons with a 'bistable firing behavior' (Figure 1a) and motor neurons with 'self-sustained firing' (Figure 1b; see text for further explanation).
22. of outstanding interest Lee RH, Heckman CJ. Systematic variation in bistability among spinal motoneurons in vivo: persistent inward currents. J Neurophysiol. 80:1998;583-593 See annotation [21].
23. Ca-L), and the current spread between the two compartments through a relatively weak coupling conductance. This is the first motor neuron model to address the systematic development of complex and bistable firing patterns by appropriate simulation of multiple ion channel blockers and neurotransmitters that account for a variety of complex firing behaviors experimentally observed in turtle motor neurons.
24. 2+ channels. Neuroscience. 61:1994;191-197.
25. Svirskis G, Hounsgaard J. Depolarization-induced facilitation of plateau-generating current in ventral horn neurons in turtle spinal cord. of special interest J Neurophysiol. 78:1997;1740-1742 This paper shows that all ventral horn interneurons and motor neurons that are able to generate plateau potentials show depolarization-induced facilitation of the underlying inward current, possibly as a result of a use-dependent facilitation of the persistent L-like calcium current. This effect corresponds to the previously described 'warm-up' effect on the plateau potential [12,24].
26. Bennett DJ, Hultborn H, Fedirchuk B, Gorassini M. Short-term plasticity in hindlimb motoneurons of decerebrate cats. J Neurophysiol. 80:1998;2038-2045.
27. Bennett DJ, Hultborn H, Fedirchuk B, Gorassini M. Synaptic activation of plateaus in hindlimb motoneurons of decerebrate cats. of outstanding interest J Neurophysiol. 80:1998;2023-2037 The authors injected current into motor neuron cell bodies through a recording electrode and found that the threshold for plateau activation under resting conditions is significantly above the threshold for recruitment of action potentials. The plateau threshold could be lowered by tonic la afferent excitation, and raised by tonic reciprocal la inhibition. Both effects were graded. Strong tonic synaptic excitation lowered the threshold sufficiently to activate the plateau at or before recruitment of action potentials. The plateau threshold was affected in a similar fashion when action potentials were inactivated. The results are consistent with a dendritic localization of the plateaux, and point to a possibly important role for plateaux in securing effective recruitment.
28. Eken T, Kiehn O. Bistable firing properties of soleus motor units in unrestrained rats. Acta Physiol Scand. 136:1989;383-394.
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30. Eken T. Spontaneous electromyographic activity in adult rat soleus muscle. of outstanding interest J Neurophysiol. 80:1998;365-377 The author studied single-motor-unit and whole-muscle EMG activity in a homogeneous slow hindlimb muscle in unrestrained rats, and found a good correlation of single-unit activity to whole-muscle EMG during locomotion. However, during tonic activity, there was an apparent dissociation between the firing in individual motor neurons, and thus between single-neuron and whole-muscle EMGs. Furthermore, there was a seemingly random recruitment of individual neurons to long-lasting firing, resulting in a cycling of activity between motor neurons over time. The behavior during tonic activity can be fully explained by the existence of motor neuron plateau potentials.
31. Kiehn O, Eker T. Prolonged firing in motor units - evidence of plateau potentials in human motoneurons? of outstanding interest J Neurophysiol. 78:1997;3061-3068 The authors studied EMG activity in human low-threshold motor neurons. They found that brief excitation of motor neurons by vibration of the homonymous muscle tendon could recruit neurons from silence to long-lasting firing in a 'preferred firing range.' Recordings from pairs of motor neurons showed that vibration-induced recruitment of one neuron to prolonged firing could happen with only transient changes in frequency in a second neuron already firing in its 'preferred firing range' - that is to say, that the prolonged firing in the first neuron was not attributable to increased activation of the whole motor neuron pool. However, unlike in the rat, a true bistable firing (i.e. shifting between two stable frequency levels) could not be demonstrated. On voluntary recruitment, neurons tended to jump directly from silence to the 'preferred firing range', making it very hard, or even impossible, to maintain steady firing at lower frequencies. It is argued that the findings are compatible with the existence of plateau potentials with a threshold close to or below the action potential threshold.
32. Gorassini M, Bennett DJ, Siu M, Yang JF. Self-sustained firing of human motor units. of outstanding interest Neurosci Lett. 247:1998;13-16 By using paired recordings of motor units, these authors confirm the findings from [31], showing that vibration-induced prolonged firing can appear in a 'test unit' without change of the firing in a 'control unit', suggesting that the prolonged firing is attributable to activation of plateau potentials rather than changes in descending drive. In addition, the duration of the prolonged firing often increased progressively after each vibration, similar to the 'warm-up' property shown for plateau potentials in turtle dorsal horn neurons and motor neurons [12,24,25] and cat motor neurons [26].
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38. m, and the cell will therefore appear more electrotonically compact for distally generated slow potentials than distally generated fast potentials.
39. Jacobs BL, Fornal CA. Activation of 5-HT neuronal activity during motor behavior. Semin Neurosci. 7:1995;401-408.