Muscle temperature has a different effect on force fluctuations in young and older women

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Abstract

Objective

To investigate the effect of muscle temperature on force fluctuations during isometric contractions in young and older females.

Methods

Fifteen young and 11 older subjects performed 3 × 30-s long submaximal isometric ankle dorsi-flexions (5%, 10%, and 15% of the maximal force). Tibialis anterior muscle temperature was monitored with an intramuscular probe and manipulated to obtain a cold, control, and warm condition. The coefficient of variation (CofV) and the relative power in the frequency bands 0–3 Hz (low), 4–6 Hz (middle), and 8–12 Hz (high) of the force signal were computed to characterise steadiness. Intramuscular EMG signals were recorded from the tibialis anterior muscle to assess motor unit discharge pattern.

Results

CofV was higher in the older than in the young subjects (P < 0.001) in all conditions. In the older group only, CofV increased with cooling with respect to control temperature (P < 0.001), whereas in the young group only, relative power of force fluctuations at high frequency decreased with cooling. Motor unit discharge rate and inter-pulse interval variability were not different between groups and across temperatures.

Conclusions

The findings indicate a different effect of temperature on the ability to maintain constant force in young and older subjects.

Significance

These results highlight the risk of further impairment to the motor control of older individuals with varying temperature.

Introduction

During a steady muscle contraction, the force output fluctuates around the target value. The amount of fluctuations is affected by factors such as age, temperature, and force (Lakie et al., 1994, Christou et al., 2002, Tracy and Enoka, 2002). Motor unit properties and the stretch reflex loop contribute to the fluctuations in force output in low-force isometric contractions. The contractile and control properties of the active motor units determine the degree of fusion of the force twitches (Christakos, 1982, Moritz et al., 2005). Additionally, during isometric contraction, the muscle spindle has been reported to respond to small force fluctuations, consequently facilitating the activation of motor units (Lippold, 1970).

Different neural mechanisms cause force fluctuations at distinct frequency bands. Allum et al. (1978) have associated the low-frequency component of the fluctuations (⩽3 Hz) with the net activity of the motor neuronal pool, including changes in the discharge rate and number of active motor units. The long and short latency stretch reflex contribute to oscillations at frequencies ∼7 and ∼10 Hz, respectively (Marsden, 1978). Similarly, the 8–10 Hz force fluctuations during isometric contraction reported by Vallbo and Wessberg (1993) were attributed to the stretch reflex.

In older individuals the force fluctuations are larger than in younger subjects (Tracy and Enoka, 2002, Vaillancourt and Newell, 2003, Bazzucchi et al., 2004) due to mechanisms not yet fully clarified. Variability in motor unit discharge rate has been identified as a critical factor in isometric force fluctuations (Moritz et al., 2005). With respect to ageing, variability in motor unit discharge rate has been shown to increase in some studies (Laidlaw et al., 2000), although this observation was not confirmed in all reports (Galganski et al., 1993, Vaillancourt et al., 2003). The amplitude of twitch force of motor units recruited at submaximal force increases with ageing (Galganski et al., 1993) but simulation studies revealed that this has negligible effects on force fluctuations (Taylor et al., 2002). The stretch reflex response is also altered with ageing. This includes a slowing of the reflex onset latency, caused by a decrease in the transmission efficiency of the signal, as well a reduction in sensitivity and number of spindles (Swash and Fox, 1972, Henderson et al., 1980, Adinolfi et al., 1991, Dewhurst et al., 2005). The contribution of a slower stretch reflex loop to the increase in force fluctuations in the older individual is, however, not known.

Temperature is an external factor that has been shown to affect the amount of force fluctuations in both healthy and diseased subjects. Everyday variations in limb muscle temperature have been reported to be ∼10 °C (Mucke and Heuer, 1989). However, studies on the effect of temperature on force fluctuations reported conflicting findings. Improvement in fine manual dexterity tasks and reduction in force fluctuation follow arm cooling in healthy young, multiple sclerosis patients and essential tremor patients (Lakie et al., 1994, Feys et al., 2005), however opposite results have been also reported (Havenith et al., 1995, Cheung et al., 2003). Temperature alters the muscle fibre membrane and contractile properties. Motor unit twitch duration increases and peak tension decreases with decreasing temperature, affecting the fusion of the tetanic output (Davies et al., 1982, Ranatunga et al., 1987). Temperature also alters the reflex response latency measured from electrical stimulation of the reflex loop (Oksa et al., 2000, Dewhurst et al., 2005) and alters spindle sensitivity in cats (Fischer and Schäfer, 1999).

There are no studies that investigated the contribution of temperature to the impaired motor control mechanisms of the older individual during fine motor tasks. The purpose of the study was, therefore, to investigate the effects of altered muscle temperature on force steadiness in low-force isometric contraction of the dorsi-flexors in young and older women.

Section snippets

Subjects

Fifteen younger (mean ± SD; age 23.6 ± 3.4 years, stature 1.64 ± 0.08 m, mass 58.0 ± 8.6 kg) and 11 older (age 68.6 ± 5.7 years, stature 1.63 ± 0.04 m, mass 70.2 ± 18.2 kg) female subjects volunteered to participate in the study. All subjects were healthy with no known neuromuscular disorders. Older subjects were medically stable according to Greig et al. (1994). All subjects were moderately active, participating in recreational physical activity no more than twice a week. All experimental tests were performed

Results

All subjects were able to maintain the target force levels for the required 30 s in all conditions. There was no effect of time on any of the variables and conditions when the contraction was split into 5-s epochs, thus data were averaged over 30 s for the following analysis.

Discussion

Young and older women performed a low-force isometric contraction under cooled, control, and warmed muscle temperature conditions. The two groups responded differently to cooling, with the older individuals increasing the force fluctuations and the younger subjects showing no change. Frequency analysis of the force fluctuations also revealed different responses of the two groups, with no sensitivity of the high-frequency band to temperature in the older, as opposed to the young, subjects.

Acknowledgment

This research was supported by a Marie Curie Fellowship of the European Community Programme “Marie Curie Training Sites” under Contract No. HPMT-CT-2000-00092.

References (49)

  • I. Bazzucchi et al.

    Differences between young and older women in maximal force, force fluctuations, and surface EMG during isometric knee extension and elbow flexion

    Muscle Nerve

    (2004)
  • W.F. Brown

    A method for estimating the number of units in thenar muscles and the changes in motor unit count with ageing

    J Neurol Neurosurg Psychiatry

    (1972)
  • S.S. Cheung et al.

    Changes in manual dexterity following short-term hand and forearm immersion in 10 ° C water

    Aviat Space Environ Med

    (2003)
  • C.N. Christakos

    A study of muscle force waveform using a population stochastic model of skeletal muscle

    Biol Cybern

    (1982)
  • E.A. Christou et al.

    Modeling of force during isometric contractions of the quadriceps femoris

    J Motor Behav

    (2002)
  • D.M. Corden et al.

    Age-related impaired reflex sensitivity in a human hand muscle

    J Neurophysiol

    (1996)
  • C.T. Davies et al.

    Contractile properties of the human triceps surae with some observations on the effects of temperature and exercise

    Eur J Appl Physiol Occup Physiol

    (1982)
  • S. Dewhurst et al.

    Temperature dependence of soleus H-reflex and M wave in young and older women

    Eur J Appl Physiol

    (2005)
  • D. Farina et al.

    Effect of temperature on spike- triggered average torque and electrophysiological properties of low-threshold motor units

    J Appl Physiol

    (2005)
  • P. Feys et al.

    Effects of peripheral cooling on intention tremor in multiple sclerosis

    J Neurol Neurosurg Psychiatry

    (2005)
  • W.R. Frontera et al.

    A cross sectional study of muscle strength and mass in 45- to 78-yr-old men and women

    J Appl Physiol

    (1991)
  • M.E. Galganski et al.

    Reduced control of motor output in a human hand muscle of elderly subjects during submaximal contractions

    J Neurophysiol

    (1993)
  • C.A. Greig et al.

    Exercise studies with elderly volunteers

    Age Ageing

    (1994)
  • G. Havenith et al.

    The hand in the cold, performance and risk

    Arctic Med Res

    (1995)
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