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J Appl Physiol 97: 225-235, 2004; doi:10.1152/japplphysiol.00066.2004
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The 1- to 2-Hz oscillations in muscle force are exacerbated by stress, especially in older adults

Evangelos A. Christou, Jennifer M. Jakobi, Ashley Critchlow, Monika Fleshner, and Roger M. Enoka

Department of Integrative Physiology, University of Colorado, Boulder, Colorado 80309-0354

Submitted 20 January 2004 ; accepted in final form 22 February 2004


   ABSTRACT
TOP
 ABSTRACT
METHODS
 RESULTS
 DISCUSSION
 GRANTS
 REFERENCES
 
Although force fluctuations during a steady contraction are often heightened in old adults compared with young adults and are enhanced in young adults during the stress response, the mechanisms underlying the augmentation are uncertain. The purpose of the study was to compare the effect of a stressor on the plasma concentrations of selected stress hormones and on the force fluctuations experienced by young and old adults during the performance of a precision grip. Thirty-six men and women (19–86 yr) participated in a protocol that comprised anticipatory (30 min), stressor (15 min), and recovery periods (25 min). The stressor was a series of noxious electrical stimuli applied to the dorsal surface of the left hand. Subjects sustained a pinch-grip force with the right hand at 2% of the maximal voluntary contraction force. The fluctuations in pinch-grip force, the interference electromyogram (EMG) of six muscles, and the spectra for the force and EMG were quantified across the 70-min protocol. The stressor increased the force fluctuations, largely due to an enhancement of the power at 1–2 Hz in the force spectrum (r2 = 0.46). The effect was greatest for the old adults compared with young and middle-aged adults. The plasma concentrations of the stress hormones (adrenocorticotropin, epinephrine, and norepinephrine) were elevated to similar levels for all three age groups, and the changes were not associated with modulation of the force fluctuations. Furthermore, the heightened EMG activity exhibited by the old adults during all periods was not related to the changes in the force fluctuations or the 1- to 2-Hz force oscillations. The absence of a change in the mean pinch-grip force during the protocol and the lack of an association between elevation of the plasma concentrations for the stress hormones and modulation of the force fluctuations suggest that the enhanced force fluctuations caused by the stressor was due to an increase in the low-frequency output of the spinal motor neurons.

force variability; electromyogram; power spectrum; pinch grip; aging

THE FORCES CONTRIBUTED BY single motor units to the net muscle force during a voluntary contraction cause the force to fluctuate about an intended value (5, 8, 10, 51). The force fluctuations vary with the intensity and type of muscle contraction, the muscle group performing the task, the level of physiological arousal, and the age and sex of the individual (13). One prominent feature of the force spectrum during submaximal isometric contractions is a distinct peak around 1–2 Hz, which experimental (8, 44, 51) and modeling (48) studies attribute to the low-frequency modulation of motor unit discharge.

We examined the physiological mechanisms that impair the steadiness of a precision grip during an intervention that heightens physiological arousal. The intervention comprised noxious electrical stimulation, which evokes a significant stress response in young adults and increases the amplitude of the force fluctuations during a submaximal pinch grip (28, 29). Amplification of the force fluctuations by the stress response may be related to an elevation of circulating stress hormones. For example, increased levels of epinephrine appear to augment the twitches from single motor units (22, 55), which can enhance the force fluctuations (48). Because older adults experience a prolonged hypothalamic-pituitary-adrenal response to stress (14, 33), we expected the noxious electrical stimulation to increase the levels of circulating stress hormones in older adults (38) and to amplify the force fluctuations more than that observed in young adults.

The purpose of the study was to compare the effect of a stressor on the plasma concentrations of selected hormones and on the force fluctuations during a precision grip in adults ranging in age from 19 to 86 yr. For all subjects, the noxious electrical stimuli increased the amplitude of the force fluctuations during the performance of a submaximal pinch-grip task. As expected, the effect was greatest in the older adults. The increase in the force fluctuations was mainly due to augmentation of the 1- to 2-Hz oscillations in pinch-grip force that were not accompanied by corresponding rhythmicities in the electromyographic (EMG) signal. In contrast to the expected results, the plasma concentrations of the stress hormones were elevated to similar levels in all subjects, and there was no association with either the amplitude of the force fluctuations or the 1- to 2-Hz oscillations in force. The spectral analysis of force suggested that the effect of the stressor on the force fluctuations likely involved modulation of the low-frequency output by the motor neurons (5, 48). Some of these results have been published previously in abstract form (4).


   METHODS
TOP
 ABSTRACT
 METHODS
RESULTS
 DISCUSSION
 GRANTS
 REFERENCES
 
Thirty-six adults (19–86 yr, 18 men and 18 women) volunteered to participate in this study (Table 1). All subjects were assessed by a physician and found to be free from neurological impairments, and they were not using medications that are known to influence neuromuscular function. Furthermore, all subjects were cognitively healthy [Pfeiffer mental status (34)], were right handed [Edinburgh Handedness Inventory (35)], had intact finger sensation [Weinstein Enhanced Sensory Test (40)], and were moderately active [Paffenbarger Physical Activity Questionnaire (31)]. In addition, all subjects had moderate levels of anxiety [>30 on the trait score of the State-Trait Anxiety Inventory (STAI) (46)] and were not depressed [<16 on Beck Inventory (47)]. The Human Research Committee at the University of Colorado in Boulder approved the procedures, and subjects provided written, informed consent before participation in the study.


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  		Table 1. Subject characteristics

 
Experimental setup.   Each subject was seated and faced an oscilloscope that was located 0.5 m away at eye level (Fig. 1). All subjects affirmed that they could see the oscilloscope display clearly. Both arms were abducted 45°, and the elbows were flexed by ~20°. Each forearm rested on the arm of the chair with the right forearm in a neutral position (halfway between forearm pronation and supination) and the left forearm pronated. The right hand and wrist were not supported, and subjects used the thumb and index fingers of the right hand to perform the pinch-grip task. The left hand was placed on the edge of the forearm support and remained relaxed throughout the experimental protocol. The electrical stimuli were delivered on the dorsal surface of the left hand, and blood samples were drawn from the antecubital vein of the left arm. Subjects were prevented from seeing their left arm and hand to minimize the stress associated with the blood draws.



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  		Fig. 1. Schematic drawing of the experimental setup. Each subject was seated and faced an oscilloscope for visual feedback. The pinch-grip task was performed with the right hand, and the electromyographic (EMG) activity of selected muscles was recorded. The electrical stimuli were delivered on the dorsal surface of the left hand, and blood samples were drawn from the antecubital vein of the left arm. Subjects were prevented from seeing their left arm and hand to minimize the stress associated with the blood draws.

 
Physiological recordings.   Subjects performed isometric contractions by pinching a force transducer (ATI Mini-40) with the thumb and index finger of the right hand. The force transducer (120 g) was 4 cm wide and had a sensitivity of 0.06 N/V. Force was sampled at 1 kHz with a 1401 plus system (Cambridge Electronic Design, Cambridge, UK), and data were stored on a computer.

The surface EMG of the right first dorsal interosseus, thenar group, flexor digitorum profundus, extensor digitorum, frontalis, and masseter muscles was measured with silver-silver chloride electrodes (4-mm diameter) that were attached to the skin with adhesive tape. Two electrodes were placed over the belly of each muscle with an interelectrode distance of 4 mm. The third electrode, which served as the reference, was placed over a bony process. The EMG signals were amplified (x1,000) with an isolated bioamplifier (S-series, Coulbourn, Allentown, PA), passed through a bandpass filter (0.13–1 kHz; S-series, Coulbourn), and sampled at 2.5 kHz (1401 plus, Cambridge Electronic Design). The lower limit for the EMG signal was set at 13 Hz because there is minimal power in the surface-detected signal below this value (12). For example, pilot experiments indicated that <3% of the total power in the spectrum for the interference EMG was located at frequencies < 20 Hz during low-force contractions, which is consistent with other reports in the literature (5, 24). The amplitude of the EMG signal was expressed as the SD of the interference EMG from each trial and was normalized to the EMG recorded during maximum isometric contractions for each muscle.

Twenty minutes before the beginning of the experimental protocol, a registered nurse inserted a plastic catheter (Saf-t-intima, Becton-Dickinson, Sandy, UT) into the left antecubital vein of each subject. Blood samples (each 15–17 ml) were obtained six times during the protocol (Fig. 2). The plasma concentrations of the hormones ACTH, epinephrine, norepinephrine, and cortisol were measured.



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  		Fig. 2. The 70-min experimental protocol. The protocol comprised anticipatory (30 min), stressor (15 min), and recovery (25 min) periods. The stressor period included three 2-min bouts in which subjects received noxious electric stimuli. During each 2-min bout, the room lights were turned on and off for 20-s intervals; the subjects received the stimuli when the lights were turned off (threat) but not when they were turned on (no threat). The threat-no threat procedure enhances the arousal response. The pinch-grip task, blood draws, State-Trait Anxiety Inventory (STAI) questionnaire, and visual analog scale (VAS) survey were performed multiple times in each period.

 
Experimental procedures.   Each subject reported to the laboratory twice. On the first visit, which lasted 30 min, subjects were familiarized with the environment and equipment, performed a maximal voluntary contraction (MVC) for the pinch-grip task, and practiced the submaximal pinch-grip task. Subjects were also instructed not to eat or drink anything except water for 2 h before the experiment that was performed on the subsequent visit. On the second visit, which lasted 120 min and always occurred in the early afternoon, subjects participated in an experimental protocol that involved anticipatory, stressor, and recovery periods (Fig. 2). After the catheter had been inserted into the antecubital vein of the left arm and before beginning the anticipatory period, each subject performed MVCs for the pinch-grip task with the right hand, and the EMG of the selected muscles was recorded. Subsequently, the threshold for the intensity of the electrical stimuli to be applied during the stressor period was determined. Once the 70-min protocol began, the cognitive indexes of stress were assessed 14 times, blood samples were obtained 6 times, and the force and EMG during the submaximal pinch-grip task were recorded 9 times (Fig. 2).

Noxious electrical stimuli.   Before the beginning of the experimental protocol, two carbon electrodes (2 cm x 2 cm) were attached to the dorsal surface of the left hand. The electrode leads were attached to a stimulator (Grass Instruments, Quincy, MA) that was used to deliver the electrical stimuli to the hand. The threshold for stimulation was determined as the minimal voltage that would evoke a twitch response in the muscles on the dorsal surface of the left hand. For each subject, the amplitude of the electrical stimuli increased with time and was 90–120 V above the predetermined threshold (Table 2). The maximal voltage applied to the hand of any subject was 160 V.


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  		Table 2. Protocol for the noxious electrical stimuli

 
MVC task.   Subjects were instructed to increase the force gradually from baseline to maximum over a 3-s period and to maintain the maximal force for ~2 s. Subjects began the task with two practice trials and then performed three trials when the force and EMG were recorded. Subsequent trials were performed if the peak forces for two of the trials differed by >5%. The trial with the highest peak force was used for analysis, and the MVC force was defined as the average force over the 0.5-s interval surrounding the peak.

Cognitive assessment of stress.   To determine the cognitive levels of anxiety and stress throughout the protocol, subjects completed both the state portion of the STAI questionnaire (46) and the visual analog scale (VAS) (16). The STAI-state questionnaire consists of 20 statements that require a response on a four-point, Likert-type scale. Each VAS (1 for anxiety and 1 for stress) consisted of a 10-cm line anchored at the far left by "not at all anxious" or "not at all stressed" and at the far right by "very anxious" or "very stressed." The right-most anchor corresponded to the most stressful or most anxious moment in the life of the subject. The subject placed a tic mark on the 10-cm line to indicate the level of anxiety or stress. Anxiety was defined as the negative feelings regarding the immediate future, whereas stress represented the physical changes (e.g., increased heart rate and perspiration) perceived by the subject. The STAI-state questionnaire was completed at the middle of the anticipatory period, at the end of the stressor period, and in the middle of the recovery period (Fig. 2). The VAS was completed five times during the anticipatory period, four times during the stressor period, and two times during the recovery period.

Hormonal assessment of stress.   Blood samples were drawn from the antecubital vein at the middle and end of the anticipatory period, after the third bout of electrical stimuli and at the end of the stressor period, and at the middle and end of the recovery period (Fig. 2). Venous blood for ACTH and cortisol was transferred into 5-ml plastic tubes (Becton Dickinson, Boston, MA). The plastic tubes for ACTH contained EDTA for an anticoagulant agent, whereas for cortisol the tubes contained sodium heparin as an anticoagulant. The samples were collected on ice, spun at 4°C at 3,000 rpm for 10 min, separated, and frozen at –20 to –80°C until tested. ACTH samples were assayed by using a chemiluminescent assay and Nichols Advantage instrument (Nichols Institute Diagnostics, San Clement, CA). The sample was not diluted, and the size aspirated by the instrument was 150 µl. Cortisol samples were assayed by using a chemiluminescent assay and the Beckman Coulter Access instrument (Beckman Coulter, Miami, FL). The sample was not diluted, and the size aspirated by the instrument was 25 µl. Venous blood for epinephrine and norepinephrine was transferred into 5-ml plastic tubes (Amersham International, Piscataway, NJ) containing EGTA and GSH as the anticoagulant and reducing agents, respectively. The samples were collected on ice and spun at 4°C, and the plasma was separated and frozen at –80°C until tested. Catecholamine levels were determined by high-performance liquid chromatography with electrochemical detection (23). Plasma volume was determined with the Evans blue dye dilution method (15).

Submaximal pinch-grip task.   Each subject pinched the force transducer with the thumb and index finger of the right hand. The subject was instructed to increase the pinch force from baseline to 2% MVC force, indicated as a solid target line on the oscilloscope, and to maintain a constant force for 60 s. The sweep time across the oscilloscope was 10 s, and the subject received visual feedback for the first 5 s of each sweep (top trace in Fig. 3). The subject was instructed to match the target force as accurately as possible and to maintain that force in the absence of visual feedback. The middle four oscilloscope sweeps of each trial were used for analysis (bottom trace in Fig. 3). For each 10-s oscilloscope sweep, force fluctuations were calculated for the last 2.3 s of visual feedback and the first 2.3 s of no visual feedback, except for the 600 ms around the removal of the visual feedback (top trace in Fig. 3). For each trial, the mean force and the fluctuations in force [SD and coefficient of variation (CV)] were averaged across the intervals that corresponded to the four oscilloscope sweeps. The pinch-grip force was measured nine times during the 70-min protocol (Fig. 2).



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  		Fig. 3. The force analysis was based on selected segments of each trial. Each subject was instructed to exert a pinch-grip force and to match a target line that was equal to 2% of the subject's maximal voluntary contraction for 60 s. There were six 10-s oscilloscope sweeps for each pinch-grip trial. For the first 5 s of each sweep, the subject was able to view both the target line and force trace (visual feedback condition), whereas for the last 5 s of each sweep, the subject viewed only the target line (no visual feedback condition). Subjects were encouraged to maintain the target force constant in the absence of visual feedback. Data from the first and last sweep were excluded from the analysis. For each of the middle 4 sweeps (sweeps 2–5), the analysis was performed on the last 2.3 s of visual feedback and the first 2.3 s of no visual feedback, except for the 600 ms around the removal of the visual feedback.

 
EMG activity.   Before beginning the experimental protocol, each subject performed maximal isometric contractions for the following tasks: abduction of the index finger (first dorsal interosseus), abduction and extension of the thumb (thenar muscles), flexion (flexor digitorum profundus) and extension (extensor digitorum) of the index finger and wrist, clenching the teeth (masseter), and a scowl with the facial muscles (frontalis). The EMG of the six muscles was recorded throughout the experimental protocol. The surface EMG was analyzed from the same periods as force. The amplitude of the EMG signal was expressed as the SD of the interference EMG (25) and was normalized to the EMG recorded during maximal isometric contractions. The power spectrum analysis of the EMG was performed on the interference EMG (see DISCUSSION for details) because rectification of the EMG signal is a nonlinear operation that has a nonuniform effect on the frequency content of the EMG signal (12).

Data analysis.   The dependent variables were the maximal force exerted with the pinch grip for the MVC task; the STAI and VAS scores for the cognitive assessment of stress; the plasma concentrations (pg/ml) of ACTH, epinephrine, norepinephrine, and cortisol for the hormonal assessment of stress; the mean force, SD of force, CV for force, and the power in the force spectrum from 0 to 12 Hz for the submaximal pinch-grip task; and the normalized amplitude of the interference EMG (%maximum) and the interference EMG spectrum from 20 to 240 Hz.

The STAI-state score was quantified by using a standardized technique (45), whereas the VAS score was indicated as the distance, in centimeters, from the left end of the 10-cm line to the tic mark made by the subject to denote the perceived level of anxiety or stress. Force fluctuations were calculated from the detrended force data and were quantified as the highest value obtained from the different trials during the anticipatory, stress, and recovery periods. A Fourier analysis was performed on the force and EMG signals, and autospectral analysis of the two signals was obtained by using Welch's averaged periodogram method with a Hanning window (no overlap) (MATLAB 6.1). The length of the data segment was 2 s. The window size for the force signal, which was sampled at 1 kHz, was 1,024, and the resolution was 0.976 Hz. The window size for the EMG signal, which was sampled at 2.5 kHz, was 512 for all contractions, which provided a resolution bin of 4.88 Hz. For statistical comparisons, the frequency data were averaged over a 1-Hz interval for force (0–12 Hz) and a 20-Hz interval for EMG (20–240 Hz). The percent power in the signal for each averaged interval was expressed as a proportion of the total power in the spectrum. The dependent variables for the spectral analysis were the median frequency, the frequency at which the peak power occurred, and the absolute and relative (%) power in the averaged bins.

Statistical analysis.   The effect of age on the MVC for the pinch grip was assessed with a bivariate correlation, whereas the sex comparison of the MVC was assessed with an independent t-test. The STAI-state scores and hormonal assessment were analyzed with a mixed two-factor analysis of covariance (ANCOVA) (2 sexes x 3 periods; age was covaried) with repeated measures on periods (SPSS version 9.0). The VAS scores were assessed with a mixed two-factor ANCOVA (2 sexes x 11 times in the 3 periods; age was covaried) with repeated measures on time. The mean force, SD of force, and CV for force was analyzed with a mixed three-factor ANCOVA (2 sexes x 3 periods x 2 visual conditions; age was covaried) with repeated measures on periods and visual conditions. The average EMG was assessed with a mixed four-factor ANCOVA (2 sexes x 3 periods x 2 visual conditions x 6 muscles; age was covaried) with repeated measures on periods and visual conditions. Because differences were expected between muscles for the EMG recordings, the average EMG of each muscle was assessed with a mixed three-factor ANCOVA (2 sexes x 3 periods x 2 visual conditions; age was covaried) with repeated measures on periods and visual conditions. The power spectrum of force (0–10 Hz) during the pinch grip was analyzed by using a mixed four-factor ANCOVA (2 sexes x 3 periods x 2 visual conditions x 11 frequency bins; age was covaried) with repeated measures on periods, visual conditions, and frequency bins. The power spectra for the surface EMG (20–240 Hz) of the first dorsal interosseus and thenar muscle group were compared by using a mixed five-factor ANCOVA (2 sexes x 3 periods x 2 muscles x 2 visual conditions x 12 frequency bins; age was covaried) with repeated measures on periods, muscles, visual conditions, and frequency bins.

Multiple linear regressions were performed in a stepwise analysis, and the associated partial correlation coefficients were used to examine the contribution of each frequency bin from the force and EMG spectra to the stress-induced increase in the force fluctuations. The statistical analysis focused on planned comparisons that examined only main effects, two-way interactions, and three-way interactions associated directly with the purpose of the study. The {alpha}-level for all statistical tests was set at 0.05, and all significant interactions were examined with appropriate post hoc analyses; these included dependent t-tests with Bonferroni corrections to locate differences between the two vision conditions and periods and independent t-tests with Bonferroni corrections to locate differences between the two sexes. Data are reported as means ± SD in the text and tables and as means ± SE in the figures.


   RESULTS
TOP
 ABSTRACT
 METHODS
 RESULTS
DISCUSSION
 GRANTS
 REFERENCES
 
The maximal pinch-grip force did not differ with the age (r2 = 0.02, P > 0.1), and it averaged 46.3 ± 2.7 N (Table 1). However, men (58.4 ± 2.7 N) were significantly stronger than women (34.3 ± 2.5 N) across the age span (P < 0.01).

Cognitive assessment.   The cognitive measures of stress increased during the stressor period compared with the anticipatory and recovery periods (period main effect, P < 0.01). State anxiety (STAI-state index) increased by ~90% (Fig. 4A), the VAS for stress increased by ~280%, and the VAS score for anxiety increased by ~250% (Fig. 4B). The state anxiety and VAS scores did not vary with age (age x period interaction, P > 0.1). However, women reported greater VAS anxiety scores (sex x time interaction, P < 0.01) during both the anticipatory and stressor periods compared with men (Fig. 4B). The three-way interaction (age x sex x period) was not significant (P > 0.1)



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  		Fig. 4. The cognitive measures of stress varied across the protocol. The STAI-state score (A) was significantly greater (*P < 0.01) during the stressor period compared with the anticipatory and recovery periods. The VAS anxiety scores (B) increased during the stressor period compared with the anticipatory and recovery periods, and the women had greater scores than the men (*P < 0.01) during both the anticipatory and stressor periods. Values are means ± SE.

 
Hormonal assessment.   Reliable blood samples were collected from 26 subjects for epinephrine, 29 subjects for norepinephrine, and 31 subjects for ACTH and cortisol. Plasma concentrations for none of the stress hormones varied with age (age main effect, P > 0.1). The concentrations for ACTH and epinephrine increased (period main effect, P < 0.01) during the stressor period compared with the anticipatory and recovery periods (Fig. 5), and the plasma concentrations of norepinephrine were greater during the stress and recovery periods compared with the anticipatory period (period main effect, P < 0.01). The plasma concentration of cortisol did not change during the protocol (P > 0.1). Averaged across the protocol, the plasma concentrations of both ACTH (34.7 ± 16.7 vs. 18.1 ± 10.9 pg/ml) and norepinephrine (437 ± 139 vs. 339 ± 109 pg/ml) were greater for men compared with women (sex main effect, P < 0.01). The two-way and three-way interactions were not significant (P > 0.1).



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  		Fig. 5. The levels of selected hormones varied across the protocol. The plasma concentrations of ACTH (A) and epinephrine (B) increased significantly (*P < 0.01) during the stressor period compared with the anticipatory and recovery periods. The plasma concentration of norepinephrine (C) was greater ({dagger}P < 0.01) during the stressor and recovery periods compared with the anticipatory period. Values are means ± SE.

 
Submaximal pinch-grip task.   The mean force exerted by all subjects during the presence (0.93 ± 0.35 N) and absence (0.92 ± 0.36 N) of visual feedback was similar (vision main effect, P > 0.1). Furthermore, the mean force (0.92 ± 0.35 N) did not vary during the experimental protocol (period main effect, P > 0.1; Fig. 6B). Apart from the expected sex differences (sex main effect, P < 0.01) on mean force, none of the other interactions were significant (P > 0.1). In contrast, the fluctuations in force increased significantly (period main effect; P < 0.01) during the stressor period compared with the anticipatory and recovery periods for both visual-feedback conditions (Fig. 6B). The SD of force increased significantly in all age groups during the stressor period (Fig. 7), especially for older adults (age x period, age x vision, and age x period x vision interactions, P < 0.01) in the absence of visual feedback period (Figs. 6A and 7). Because the absolute force exerted during the submaximal pinch-grip task was greater in men (1.14 ± 0.27 N) compared with women (0.71 ± 0.29 N), the force fluctuations were normalized to the mean force as the CV. The CV for force was greater for women compared with men (sex main effect and sex x period interaction, P < 0.01) during the anticipatory (2.63 ± 1.61 vs. 1.96 ± 0.76%) and stressor periods (4.44 ± 3.99 vs. 3.22 ± 1.92%). The CV for force also increased with age (age x period and age x period x vision interaction, P < 0.01), especially during the stressor period. For example, the CV for force for old adults was 2.92 ± 1.86% during the anticipatory period compared with 2.00 ± 0.68% for young adults, whereas the CV for force was 5.62 ± 4.57% for old adults during the stressor period and 2.45 ± 0.86% for young adults. The other interactions were not significant (P > 0.1).



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  		Fig. 6. The force exerted during the submaximal pinch-grip task. A: representative force recordings for 1 young subject and 1 old subject during the anticipatory, stressor, and recovery periods. These recordings were obtained in the absence of visual feedback. B: although the mean force did not vary across the 3 phases of the protocol, the SD of force increased by ~22% (*P < 0.01) during the stressor period compared with anticipatory and recovery periods. Values are means ± SE.

 


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  		Fig. 7. The SD of force varied with the phase of the protocol and subject age. A: no visual feedback. B: visual feedback. Values are means ± SE. The SD of force increased with age during all 3 periods of the protocol. For each age group, the SD of force was greater during the stressor period compared with the anticipatory and recovery periods. The increase in the SD of force during the stressor period was greater in the absence of visual feedback, especially for the older adults. *P < 0.05 for the stressor period compared with anticipatory and recovery periods. {dagger}P < 0.05 for the old adults compared with young adults.

 
Force spectrum.   The median frequency for the force spectrum was 1.17 ± 0.13 Hz in the presence of visual feedback and 1.02 ± 0.04 Hz in the absence of visual feedback (P > 0.1). The total power in the force spectrum, especially at 1–2 Hz, was greater during the stressor period compared with the other two periods (period main effect and period x frequency interaction, P < 0.01). Power in the 1- to 2-Hz range of the force spectrum increased with age (age main effect, P < 0.01) during all three phases of the protocol (Fig. 8B), and only the older adults exhibited a secondary peak at 5–10 Hz (P < 0.01) (inset in Fig. 8A). Furthermore, the effect of age on the power at 1–2 Hz (Fig. 8B) and at 5–10 Hz was enhanced during the stressor period (age x period, age x frequency, and age x period x frequency interactions, P < 0.01). When the distribution of power in the force spectrum was normalized to the total power in the spectrum, women exhibited significantly greater power (sex x frequency interaction, P < 0.01) from 1 to -2 Hz compared with men (51.6 ± 7.7 vs. 46.3 ± 11.0%) and significantly less power at 5–10 Hz (0.92 ± 0.68 vs. 2.0 ± 1.44%). None of the other main effects and interactions were significant (P > 0.1).



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  		Fig. 8. The power spectra for force. A: representative force spectra for young (19–34 yr), middle-aged (41–61 yr), and old adults (66–86 yr). Most of the power occurred from 1 to 2 Hz and increased with age during all 3 phases of the protocol. A secondary peak in the 5- to 10-Hz band was present in the data from old adults but not in that from young or middle-aged adults (inset). B: exposure to the noxious stressor increased power at 1–2 Hz for all subjects, especially in older adults. Values are means ± SE.

 
Muscle activity.   The normalized amplitude of the surface EMG from the extensor digitorum (18.5 ± 10.5%), frontalis (17.0 ± 14.2%), masseter (8.29 ± 20.8%), and first dorsal interosseus (9.64 ± 22.2%) muscles was similar for all subjects (age, sex, and vision main effects, P > 0.05), whereas the surface EMG for the flexor digitorum profundus and thenar muscles increased significantly with age (age main effect, P < 0.01). The EMG amplitude for the thenar muscles, for example, was 4.52 ± 4.10% for the young subjects and 13.8 ± 14.4% for the old subjects. The normalized EMG amplitude for these muscles did not vary across the experimental protocol (period main effect, P > 0.05). All other interactions were not significant (P > 0.1).

The median frequency for the interference EMG spectra, which did not differ with age, muscle, or protocol period (P > 0.1), was 94.7 ± 21.1 Hz for first dorsal interosseus and 94.1 ± 15.7 Hz for the thenar muscles. The power in both EMG spectra increased with age (age main effect, P < 0.01; Fig. 9A, B). The age differences in the EMG spectra were greater at 90–180 Hz (age x muscle x frequency interaction, P < 0.01), especially for the thenar muscles (Fig. 9C). All other interactions were not significant (P > 0.1).



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  		Fig. 9. The power spectra for the surface EMG. Representative EMG spectra (averaged across protocol periods) for the first dorsal interosseus (FDI; A) and thenar (B) muscles. Values are means ± SE. For the first dorsal interosseus muscle, old adults (66–86 yr) exhibited greater EMG power compared with young (19–34 yr) and middle-aged adults (41–61 yr). For the thenar muscle, however, old and middle-aged adults exhibited greater EMG power than young adults. Power from 90–180 Hz increased significantly with age for both muscles (C), although the relations were rather weak (r2 = 0.12 and r2 = 0.08).

 
Associations between force fluctuations and stress response.   Multiple regression analysis indicated that the significant relation between the SD of force and the modulation of power in the force spectrum (r2 = 0.57, P < 0.0001) was mainly due to a contribution from the power at 1–2 Hz (r2 change = 0.46, P < 0.0001; Fig. 10), but it also included a contribution from the power at 9–10 Hz (r2 change = 0.11, P < 0.0001). The SD of force was not associated with EMG amplitude of the first dorsal interosseus (r2 = 0.001, P > 0.1) or thenar (r2 = 0.01, P > 0. 1) muscles. Although the SD of force was weakly associated with EMG spectra and the plasma concentrations of the ACTH hormone, none of the measures was significantly associated with the power in the force spectrum at 1–2 Hz (P > 0.1). Increases in ACTH plasma concentration were weakly associated with the SD of force (r2 = 0.14, P < 0.01). None of the other cognitive (STAI-state, VAS), hormonal (epinephrine, norepinephrine, cortisol), or EMG measures were significantly associated with either the SD of force or the 1- to 2-Hz oscillations in force (P > 0.1).



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  		Fig. 10. The relation between force fluctuations and low-frequency power in the force spectra. Each data point represents a pair of values from 1 of the 3 protocol periods (anticipatory, stressor, or recovery) for 1 subject. The amount of power at 1–2 Hz in the force spectrum was linearly related to the variability in force. The relation indicates that oscillations in the force at 1–2 Hz accounted for 46% of the variability in the SD of force (r2 = 0.46, P < 0.001). In contrast, the association between the EMG amplitude and SD of force was not significant (P > 0.1).

 

   DISCUSSION
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This study examined the effects of a stressor on the plasma concentrations of selected hormones and on modulation of the force fluctuations when adults, ranging in age from 19 to 86 yr, performed a precision grip. The fluctuations in force during the submaximal contraction, which were quantified as the SD of force, increased during presentation of the stressor (noxious electric stimuli), as observed previously (28, 29). The new findings included the observation that the effect of the stressor on the force fluctuations was greater in older adults, the elevation of plasma concentrations for selected hormones during the stressor period was similar for all ages, the enhanced fluctuations in force were largely due to oscillations at 1–2 Hz, and the force fluctuations were not accompanied by a corresponding modulation of power in the interference EMG spectra.

Modulation of the force fluctuations.   In contrast with the 6- to 12-Hz oscillations observed during postural contractions and slow movements (18, 53), experimental studies have found that the fluctuations in muscle force during isometric contractions performed against a rigid restraint include a significant component at ~2 Hz (8, 44, 51). Because the low-frequency oscillations in force are accompanied by coherent modulation of motor unit discharge at low frequencies (0–2 Hz), the fluctuations in force are often presumed to reflect rhythmicities that are inherent in the descending drive onto the motor neuron pool (3, 7, 51). Such a scheme, however, assumes that all motor neurons in the pool respond similarly to the common synaptic input (48) and that the correlated output is not a consequence of intrinsic neuronal properties, such as those that can be caused by active dendritic conductances (11, 54).

Computer simulations with models of motor unit recruitment and rate coding have demonstrated the presence of low-frequency oscillations in the simulated force even when the discharge times of action potentials by the activated motor units were independent (48). The low-frequency peak in the power spectrum for the simulated force with asynchronous discharges, however, was not as prominent as that observed in experimental records for the first dorsal interosseus muscle. The match between the spectra for the experimental and simulated forces was improved by the imposition of a 1-Hz oscillation on the simulated discharge times. The 1-Hz oscillation model matched the experimental measurements by producing maximal power at low frequencies (0.99 and 1.37 Hz, respectively), the percentage of maximal power at that frequency (38 and 43%, respectively), and a decline in the median frequency with increasing force (0.98 to 0.10 Hz and 1.47 to 0.22 Hz, respectively). Models that manipulated the levels of discharge rate variability, motor unit synchronization, and higher frequency (12 and 20 Hz) oscillations also exhibited a significant low-frequency component. However, no model was completely successful in replicating the distribution of power in the experimental force spectrum. Because the only feature that was consistent across these models was the process of summation of motor unit twitches to produce whole muscle force, it was concluded that part of the power from 0 to 2 Hz was due to the mechanical summation of the motor unit twitches.

The findings of the present study, in combination with this previous modeling work (48), suggest that the increased force fluctuations due to the noxious stressor were attributable to augmentation of the low-frequency oscillations in motor output from the spinal cord. Although the distribution of power in the force spectrum is influenced by the mechanical summation of motor unit forces, the absence of a change in the mean force across the 70-min protocol indicates that the increase in the force fluctuations was not caused by augmentation of the motor unit forces. Rather, the efficacy of the 1-Hz oscillation model at matching the experimental measurements provides a compelling case for low-frequency modulation of motor unit discharge. However, the relative contributions of common synaptic input and intrinsic neuronal properties to the modulation of motor output remain uncertain (49).

EMG activity.   The noxious electrical stimuli did not have a significant effect on EMG amplitude during the submaximal pinch grip. Although the EMG amplitude for the thenar and flexor digitorum profundus muscles was greater for the older adults and the EMG spectra for the thenar and first dorsal interosseus muscles varied with age and level of stress, neither the amplitude nor the spectral characteristics of the surface EMG were associated with force fluctuations or the 1- to 2-Hz oscillations in force.

The absence of an association between the surface EMG and the force fluctuations was not due to the use of the interference instead of the rectified EMG. Although the rectified EMG has been used extensively as a method to enhance the low-frequency peaks and hence the detection of average discharge rates of motor units, this approach does not seem appropriate given the limitations of the surface EMG and the distortion that is introduced by rectifying the signal (12). Simulation of the surface EMG at different levels of muscle activation indicated that, when the discharge characteristics of the activated motor units matched those observed experimentally, the peaks in the rectified EMG spectra failed to identify the average discharge rate of the motor units and additional low-frequency peaks were introduced in the spectrum (Fig. 4 in Ref. 12). In contrast, average motor unit discharge was often evident in the peaks of the interference EMG spectra but not the rectified EMG. Nonetheless, analysis of the rectified EMG spectra for the data presented in this report did not alter the findings observed with the interference EMG (data not reported).

Some studies suggest that the surface EMG cannot be used to detect low-frequency oscillations in motor unit discharge during voluntary contractions. For example, concentric and eccentric contractions of the first dorsal interosseus muscle at various movement speeds were associated with 6- to 12-Hz oscillations in index finger acceleration that were not associated with the interference or rectified surface EMG (5). Furthermore, coherent oscillations between activity in higher centers (measured with magnetoencephalography) and the rectified EMG appear to be ~20 Hz (39) and not at lower frequencies (<5 Hz). In addition, low-frequency oscillations recorded at cortical and pyramidal levels (<5 Hz) were not consistently associated with the spectrum of the rectified surface EMG (1). Rather, the frequency characteristics of motor unit discharge appear to be more effectively represented in the low-frequency oscillations in force rather than the surface EMG (7, 8, 19, 51).

Cognitive and physiological responses to the stressor.   The noxious electrical stimuli applied to the back of the left hand were successful in elevating both cognitive and physiological measures of stress. All subjects (no age effect) reported an increase in the perceived levels of stress and anxiety, and exhibited an increase in the plasma concentrations of hormones typically associated with acute stress (ACTH, epinephrine, norepinephrine). These findings contrast with the expectation that older adults would experience heightened activity in the hypothalamic-pituitary-adrenal axis in response to stress (14, 33), but they are consistent with previous studies that indicate a similar change in the plasma concentration of various hormones in response to acute stress for young and old adults (6, 50).

The plasma concentrations of the stress hormones, however, provide only limited information about the central effects of the noxious stimuli. For example, these measurements provide no information about the efficacy of the hormones at the site of action, and circulating measures of norepinephrine do not accurately reflect neural activation of the sympathetic nervous system in specific tissues (41). One intriguing possibility is the influence that the sympathetic nervous system might exert on the muscle spindle (37) during a steady contraction. Elevated levels of stress increase sympathetic activity (27), which appears to decrease the resting discharge rate of muscle spindle afferents and potentially lowers the excitability of {alpha}- and {gamma}-motor neurons (37).

Enhanced oscillations in older adults.   The force fluctuations experienced by the subjects during the pinch grip increased with age during all three periods of the protocol (anticipatory, stressor, and recovery). This difference was most pronounced during the stressor period and was associated with an augmentation of the fluctuations at 1–2 Hz and 5–9 Hz (Figs. 5A, 6, and 7A). A recent study (52) also found that the fluctuations in index finger force during a constant-force contraction with the first dorsal interosseus muscle were greater for old adults due to an increase in the power in the <4-Hz band. Based on previous experimental studies (8, 51) and a modeling study (48), enhancement of the 1- to 2-Hz band suggests an increase in the strength of the low-frequency oscillations in motor unit discharge, whereas the modulation at 5–9 Hz is consistent with an increase in the number of motor units discharging at about the same rate. The greater coherence (5–9 Hz) in motor unit discharge exhibited by old adults (43) was presumably further enhanced by the noxious electrical stimuli.

Low-frequency modulation of motor unit discharge is often presumed to arise from rhythmicities in the descending drive to the motor neuron pool (2). For example, pyramidal tract neurons displayed the greatest amount of coherence at ≤3 Hz and moderate levels of coherence in higher frequency bands (10–14, 17–31, 34–44 Hz) when monkeys performed a precision pinch grip (1). The force fluctuations experienced by older adults during the stress response may relate to a reduced ability to modulate the descending drive using sensory feedback. Independent of age, exposure to a stressor reduces sensory feedback from the muscle spindles (36, 37), which could result in fewer adjustments in the low-frequency modulation of motor unit discharge (descending drive) and enhance the force fluctuations. Sensory feedback from muscle spindles also declines with advancing age (26), which might increase the effects of stress on the descending drive. For example, the reduced ability of older adults to use sensory feedback and to rely more on visual feedback (42) to modulate the descending drive might underlie the effect shown in Fig. 6. Conversely, the low-frequency modulation of spinal cord output could arise from active calcium conductances in the neurons (11, 54).

Sex differences in the stress response.   Women, independent of age, exhibited greater force fluctuations and 1- to 2-Hz oscillations compared with men. These findings are consistent with previous reports of young women exhibiting increased force fluctuations during the stress response (28, 29). However, the present findings dissociate differential levels of circulating stress hormones, alternative muscle activation, and estrogen levels as potential physiological mechanisms for the greater force fluctuations experienced by women. The plasma concentrations of the stress hormones (except for ACTH, which was higher in men) and muscle activation patterns were similar for men and women. Furthermore, the absence of an interaction between sex and age suggest that estrogen levels did not influence the motor performance.

Consistent with other reports of women often perceiving noxious stimuli as more intense than men (17, 21), the electrical stimuli created more anxiety in the women compared with men (Fig. 3B). Sex differences in the perception of noxious stimuli are not associated with differences in either body size and skin thickness (20) or social expectations (13, 30). Rather, there is evidence that the underlying sex differences are related to central neural mechanisms that mediate the perception of the noxious stimuli. For example, a noxious heat stimulus (50°C) on the hand was perceived by women as more intense and was associated with greater activation of the contralateral thalamus and anterior insula (32). Furthermore, when tonic pressure was applied to the fingers of young adults, women reported greater pain than men, and their responses were highly associated with pupil dilation (9). Such observations suggest that the women experienced a greater activation of higher centers during the noxious electrical stimuli, which led to an amplified input to the motor neuron pool and greater 1- to 2-Hz oscillations in force.

In summary, the noxious stressor increased force fluctuations, especially the 1- to 2-Hz oscillations in force, and these were greater for old adults and for women. Although the levels of some stress hormones were elevated during the stress response, the plasma concentrations of stress hormones could not explain the age and sex differences. These differences could also not be explained by changes in either the amplitude or frequency characteristics of the surface EMG. The only physiological mechanism that appears to explain the age and sex differences in the stress-induced enhancement of the 1- to 2-Hz oscillations in force is an augmentation of the low-frequency modulation of motor unit discharge.


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This work was supported by National Institutes of Health (NIH) Awards AG-09000 and AG-20339 (to R. M. Enoka) and NIH Grant 2 M01-RR-00051 General Clinical Research Center Program of the National Center for Research Resources.


   FOOTNOTES
 

Address for reprint requests and other correspondence: E. A. Christou, Dept. of Integrative Physiology, University of Colorado, Boulder, CO 80309-0354 (E-mail: echristo{at}colorado.edu).

The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.


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