Contractile properties of single motor units in human toe extensors assessed by intraneural motor axon stimulation

Vaughan G. Macefield, Andrew J Fuglevand, Brenda Bigland-Ritchie

Research output: Contribution to journalArticle

94 Citations (Scopus)

Abstract

1. Single motor axons innervating human toe extensor muscles were selectively stimulated through a tungsten microelectrode inserted percutaneously into the peroneal nerve. Twitch and tetanic forces were measured from a strain gauge over the proximal phalanx of the toe generating the greatest force. Twitch data were obtained from 19 single motor units in nine subjects: 8 motor units supplied extensor hallucis longus (EHL), 5 motor units supplied extensor digitorum longus (EDL), and 6 motor units supplied extensor digitorum brevis (EDB). Unpotentiated twitch forces ranged from 6.3 to 78.1 mN (20.0 ± 4.0 mN, mean ± SE), with the distribution highly skewed toward small forces. Twitch contraction and half-relaxation times were 74.8 ± 3.9 and 78.6 ± 6.0 ms, respectively. Compared with motor units in human thenar muscles, those in human toe extensor muscles were stronger but slower. However, as in thenar motor units, twitch force and contraction time were not related. 2. Force-frequency relationships were determined for 13 units (5 EDL, 5 EHL, 3 EDB) by stimulating each unit with short trains (1.0-5.0 s) of constant frequency (2-100 Hz). Peak force was related to stimulus frequency in a sigmoid fashion. The steep region of the curve extended from 5.5 ± 0.7 (SE) Hz to 16.3 ± 1.1 Hz for all units, and the stimulus frequency required to generate half-maximal force (9.6 ± 0.6 Hz) was close to the center of the steep range. This frequency, which was inversely related to twitch contraction time, was lower than the frequency required to develop half- maximal force of human thenar motor units (12 ± 4 Hz, mean ± SD). The slopes of the regression lines relating force to frequency, computed over the steep range for each unit, were also lower for the toe extensors (3.7 ± 0.7 mN/Hz) than for the thenar muscles (6 ± 1 mN/Hz). 3. Maximal tetanic forces ranged from 29.9 to 188.1 mN (89.0 ± 16.5 mN, mean ± SE), and were generated at stimulus frequencies from 15 to 100 Hz (median 50 Hz). The simulation frequency required for fused tetani (absence of noticeable force fluctuation) was generally less than that required for maximum tetanic force. The mean twitch-tetanus ratio, calculated for unpotentiated twitches, was 0.22 ± 0.02 (range 0.15-0.41). This ratio was higher than for human thenar motor units (0.14 ± 0.06, mean ± SE). After twitch potentiation of 10 units, the mean twitch-tetanus ratio increased to 0.28 ± 0.04. 4. The effects of preceding each stimulus train with a short interstimulus interval (10 ms) on force production at each frequency were examined in nine motor units. Peak forces at the onset of each contraction were higher when such an 'initial doublet' preceded stimulus trains of ≤20 Hz, but the mean force at the end of each stimulus train was not significantly affected at any frequency. 5. Eight units were stimulated with a train that increased in frequency continuously from 2 to 80 Hz, and then decreased symmetrically. This pattern resulted in peak forces that were higher on the descending limb of the stimulus train, the force-frequency relationship tracing a hysteresis loop. Hysteresis was exhibited because damping in the neuromuscular system causes the mechanical output of muscle to lag behind neural input. Thus, in non-steady-state conditions (as in most forms of natural activity), somewhat higher firing rates may be required to attain a particular level of force; once attained, force output will be transiently unresponsive to diminution of firing rate. 6. We conclude that there are differences in the contractile properties of single motor units in human toe extensor muscles (involved in posture and locomotion) and thenar muscles (involved in prehension and manipulation). Twitch-tetanus ratios were greater for motor units in the toe extensors, and this property accounted for the lower force sensitivity of these units to increases in frequency. Because of their slower twitches, the toe extensor motor units required lower excitation frequencies to generate half-maximal tetanic force.

Original languageEnglish (US)
Pages (from-to)2509-2519
Number of pages11
JournalJournal of Neurophysiology
Volume75
Issue number6
StatePublished - Jun 1996
Externally publishedYes

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Toes
Axons
Muscles
Tetanus
Toe Phalanges
Peroneal Nerve
Tungsten
Microelectrodes
Sigmoid Colon
Locomotion
Posture
Extremities

ASJC Scopus subject areas

  • Physiology
  • Neuroscience(all)

Cite this

Contractile properties of single motor units in human toe extensors assessed by intraneural motor axon stimulation. / Macefield, Vaughan G.; Fuglevand, Andrew J; Bigland-Ritchie, Brenda.

In: Journal of Neurophysiology, Vol. 75, No. 6, 06.1996, p. 2509-2519.

Research output: Contribution to journalArticle

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title = "Contractile properties of single motor units in human toe extensors assessed by intraneural motor axon stimulation",
abstract = "1. Single motor axons innervating human toe extensor muscles were selectively stimulated through a tungsten microelectrode inserted percutaneously into the peroneal nerve. Twitch and tetanic forces were measured from a strain gauge over the proximal phalanx of the toe generating the greatest force. Twitch data were obtained from 19 single motor units in nine subjects: 8 motor units supplied extensor hallucis longus (EHL), 5 motor units supplied extensor digitorum longus (EDL), and 6 motor units supplied extensor digitorum brevis (EDB). Unpotentiated twitch forces ranged from 6.3 to 78.1 mN (20.0 ± 4.0 mN, mean ± SE), with the distribution highly skewed toward small forces. Twitch contraction and half-relaxation times were 74.8 ± 3.9 and 78.6 ± 6.0 ms, respectively. Compared with motor units in human thenar muscles, those in human toe extensor muscles were stronger but slower. However, as in thenar motor units, twitch force and contraction time were not related. 2. Force-frequency relationships were determined for 13 units (5 EDL, 5 EHL, 3 EDB) by stimulating each unit with short trains (1.0-5.0 s) of constant frequency (2-100 Hz). Peak force was related to stimulus frequency in a sigmoid fashion. The steep region of the curve extended from 5.5 ± 0.7 (SE) Hz to 16.3 ± 1.1 Hz for all units, and the stimulus frequency required to generate half-maximal force (9.6 ± 0.6 Hz) was close to the center of the steep range. This frequency, which was inversely related to twitch contraction time, was lower than the frequency required to develop half- maximal force of human thenar motor units (12 ± 4 Hz, mean ± SD). The slopes of the regression lines relating force to frequency, computed over the steep range for each unit, were also lower for the toe extensors (3.7 ± 0.7 mN/Hz) than for the thenar muscles (6 ± 1 mN/Hz). 3. Maximal tetanic forces ranged from 29.9 to 188.1 mN (89.0 ± 16.5 mN, mean ± SE), and were generated at stimulus frequencies from 15 to 100 Hz (median 50 Hz). The simulation frequency required for fused tetani (absence of noticeable force fluctuation) was generally less than that required for maximum tetanic force. The mean twitch-tetanus ratio, calculated for unpotentiated twitches, was 0.22 ± 0.02 (range 0.15-0.41). This ratio was higher than for human thenar motor units (0.14 ± 0.06, mean ± SE). After twitch potentiation of 10 units, the mean twitch-tetanus ratio increased to 0.28 ± 0.04. 4. The effects of preceding each stimulus train with a short interstimulus interval (10 ms) on force production at each frequency were examined in nine motor units. Peak forces at the onset of each contraction were higher when such an 'initial doublet' preceded stimulus trains of ≤20 Hz, but the mean force at the end of each stimulus train was not significantly affected at any frequency. 5. Eight units were stimulated with a train that increased in frequency continuously from 2 to 80 Hz, and then decreased symmetrically. This pattern resulted in peak forces that were higher on the descending limb of the stimulus train, the force-frequency relationship tracing a hysteresis loop. Hysteresis was exhibited because damping in the neuromuscular system causes the mechanical output of muscle to lag behind neural input. Thus, in non-steady-state conditions (as in most forms of natural activity), somewhat higher firing rates may be required to attain a particular level of force; once attained, force output will be transiently unresponsive to diminution of firing rate. 6. We conclude that there are differences in the contractile properties of single motor units in human toe extensor muscles (involved in posture and locomotion) and thenar muscles (involved in prehension and manipulation). Twitch-tetanus ratios were greater for motor units in the toe extensors, and this property accounted for the lower force sensitivity of these units to increases in frequency. Because of their slower twitches, the toe extensor motor units required lower excitation frequencies to generate half-maximal tetanic force.",
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N2 - 1. Single motor axons innervating human toe extensor muscles were selectively stimulated through a tungsten microelectrode inserted percutaneously into the peroneal nerve. Twitch and tetanic forces were measured from a strain gauge over the proximal phalanx of the toe generating the greatest force. Twitch data were obtained from 19 single motor units in nine subjects: 8 motor units supplied extensor hallucis longus (EHL), 5 motor units supplied extensor digitorum longus (EDL), and 6 motor units supplied extensor digitorum brevis (EDB). Unpotentiated twitch forces ranged from 6.3 to 78.1 mN (20.0 ± 4.0 mN, mean ± SE), with the distribution highly skewed toward small forces. Twitch contraction and half-relaxation times were 74.8 ± 3.9 and 78.6 ± 6.0 ms, respectively. Compared with motor units in human thenar muscles, those in human toe extensor muscles were stronger but slower. However, as in thenar motor units, twitch force and contraction time were not related. 2. Force-frequency relationships were determined for 13 units (5 EDL, 5 EHL, 3 EDB) by stimulating each unit with short trains (1.0-5.0 s) of constant frequency (2-100 Hz). Peak force was related to stimulus frequency in a sigmoid fashion. The steep region of the curve extended from 5.5 ± 0.7 (SE) Hz to 16.3 ± 1.1 Hz for all units, and the stimulus frequency required to generate half-maximal force (9.6 ± 0.6 Hz) was close to the center of the steep range. This frequency, which was inversely related to twitch contraction time, was lower than the frequency required to develop half- maximal force of human thenar motor units (12 ± 4 Hz, mean ± SD). The slopes of the regression lines relating force to frequency, computed over the steep range for each unit, were also lower for the toe extensors (3.7 ± 0.7 mN/Hz) than for the thenar muscles (6 ± 1 mN/Hz). 3. Maximal tetanic forces ranged from 29.9 to 188.1 mN (89.0 ± 16.5 mN, mean ± SE), and were generated at stimulus frequencies from 15 to 100 Hz (median 50 Hz). The simulation frequency required for fused tetani (absence of noticeable force fluctuation) was generally less than that required for maximum tetanic force. The mean twitch-tetanus ratio, calculated for unpotentiated twitches, was 0.22 ± 0.02 (range 0.15-0.41). This ratio was higher than for human thenar motor units (0.14 ± 0.06, mean ± SE). After twitch potentiation of 10 units, the mean twitch-tetanus ratio increased to 0.28 ± 0.04. 4. The effects of preceding each stimulus train with a short interstimulus interval (10 ms) on force production at each frequency were examined in nine motor units. Peak forces at the onset of each contraction were higher when such an 'initial doublet' preceded stimulus trains of ≤20 Hz, but the mean force at the end of each stimulus train was not significantly affected at any frequency. 5. Eight units were stimulated with a train that increased in frequency continuously from 2 to 80 Hz, and then decreased symmetrically. This pattern resulted in peak forces that were higher on the descending limb of the stimulus train, the force-frequency relationship tracing a hysteresis loop. Hysteresis was exhibited because damping in the neuromuscular system causes the mechanical output of muscle to lag behind neural input. Thus, in non-steady-state conditions (as in most forms of natural activity), somewhat higher firing rates may be required to attain a particular level of force; once attained, force output will be transiently unresponsive to diminution of firing rate. 6. We conclude that there are differences in the contractile properties of single motor units in human toe extensor muscles (involved in posture and locomotion) and thenar muscles (involved in prehension and manipulation). Twitch-tetanus ratios were greater for motor units in the toe extensors, and this property accounted for the lower force sensitivity of these units to increases in frequency. Because of their slower twitches, the toe extensor motor units required lower excitation frequencies to generate half-maximal tetanic force.

AB - 1. Single motor axons innervating human toe extensor muscles were selectively stimulated through a tungsten microelectrode inserted percutaneously into the peroneal nerve. Twitch and tetanic forces were measured from a strain gauge over the proximal phalanx of the toe generating the greatest force. Twitch data were obtained from 19 single motor units in nine subjects: 8 motor units supplied extensor hallucis longus (EHL), 5 motor units supplied extensor digitorum longus (EDL), and 6 motor units supplied extensor digitorum brevis (EDB). Unpotentiated twitch forces ranged from 6.3 to 78.1 mN (20.0 ± 4.0 mN, mean ± SE), with the distribution highly skewed toward small forces. Twitch contraction and half-relaxation times were 74.8 ± 3.9 and 78.6 ± 6.0 ms, respectively. Compared with motor units in human thenar muscles, those in human toe extensor muscles were stronger but slower. However, as in thenar motor units, twitch force and contraction time were not related. 2. Force-frequency relationships were determined for 13 units (5 EDL, 5 EHL, 3 EDB) by stimulating each unit with short trains (1.0-5.0 s) of constant frequency (2-100 Hz). Peak force was related to stimulus frequency in a sigmoid fashion. The steep region of the curve extended from 5.5 ± 0.7 (SE) Hz to 16.3 ± 1.1 Hz for all units, and the stimulus frequency required to generate half-maximal force (9.6 ± 0.6 Hz) was close to the center of the steep range. This frequency, which was inversely related to twitch contraction time, was lower than the frequency required to develop half- maximal force of human thenar motor units (12 ± 4 Hz, mean ± SD). The slopes of the regression lines relating force to frequency, computed over the steep range for each unit, were also lower for the toe extensors (3.7 ± 0.7 mN/Hz) than for the thenar muscles (6 ± 1 mN/Hz). 3. Maximal tetanic forces ranged from 29.9 to 188.1 mN (89.0 ± 16.5 mN, mean ± SE), and were generated at stimulus frequencies from 15 to 100 Hz (median 50 Hz). The simulation frequency required for fused tetani (absence of noticeable force fluctuation) was generally less than that required for maximum tetanic force. The mean twitch-tetanus ratio, calculated for unpotentiated twitches, was 0.22 ± 0.02 (range 0.15-0.41). This ratio was higher than for human thenar motor units (0.14 ± 0.06, mean ± SE). After twitch potentiation of 10 units, the mean twitch-tetanus ratio increased to 0.28 ± 0.04. 4. The effects of preceding each stimulus train with a short interstimulus interval (10 ms) on force production at each frequency were examined in nine motor units. Peak forces at the onset of each contraction were higher when such an 'initial doublet' preceded stimulus trains of ≤20 Hz, but the mean force at the end of each stimulus train was not significantly affected at any frequency. 5. Eight units were stimulated with a train that increased in frequency continuously from 2 to 80 Hz, and then decreased symmetrically. This pattern resulted in peak forces that were higher on the descending limb of the stimulus train, the force-frequency relationship tracing a hysteresis loop. Hysteresis was exhibited because damping in the neuromuscular system causes the mechanical output of muscle to lag behind neural input. Thus, in non-steady-state conditions (as in most forms of natural activity), somewhat higher firing rates may be required to attain a particular level of force; once attained, force output will be transiently unresponsive to diminution of firing rate. 6. We conclude that there are differences in the contractile properties of single motor units in human toe extensor muscles (involved in posture and locomotion) and thenar muscles (involved in prehension and manipulation). Twitch-tetanus ratios were greater for motor units in the toe extensors, and this property accounted for the lower force sensitivity of these units to increases in frequency. Because of their slower twitches, the toe extensor motor units required lower excitation frequencies to generate half-maximal tetanic force.

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