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. 2019 Nov 27;123(2):522–528. doi: 10.1152/jn.00349.2019

The effects of forearm position and contraction intensity on cortical and spinal excitability during a submaximal force steadiness task of the elbow flexors

Alexandra F Yacyshyn 1, Samantha Kuzyk 1, Jennifer M Jakobi 1,*,✉, Chris J McNeil 1,*
PMCID: PMC7052633  PMID: 31774348

Abstract

Elbow flexor force steadiness is less with the forearm pronated (PRO) compared with neutral (NEU) or supinated (SUP) and may relate to neural excitability. Although not tested in a force steadiness paradigm, lower spinal and cortical excitability was observed separately for biceps brachii in PRO, possibly dependent on contractile status at the time of assessment. This study aimed to investigate position-dependent changes in force steadiness as well as spinal and cortical excitability at a variety of contraction intensities. Thirteen males (26 ± 7 yr; means ± SD) performed three blocks (PRO, NEU, and SUP) of 24 brief (~6 s) isometric elbow flexor contractions (5, 10, 25 or 50% of maximal force). During each contraction, transcranial magnetic stimulation or transmastoid stimulation was delivered to elicit a motor-evoked potential (MEP) or cervicomedullary motor-evoked potential (CMEP), respectively. Force steadiness was lower in PRO compared with NEU and SUP (P ≤ 0.001), with no difference between NEU and SUP. Similarly, spinal excitability (CMEP/maximal M wave) was lower in PRO than NEU (25 and 50% maximal force; P ≤ 0.010) and SUP (all force levels; P ≤ 0.004), with no difference between NEU and SUP. Cortical excitability (MEP/CMEP) did not change with forearm position (P = 0.055); however, a priori post hoc testing for position showed excitability was 39.8 ± 38.3% lower for PRO than NEU at 25% maximal force (P = 0.006). The data suggest that contraction intensity influences the effect of forearm position on neural excitability and that reduced spinal and, to a lesser extent, cortical excitability could contribute to lower force steadiness in PRO compared with NEU and SUP.

NEW & NOTEWORTHY To address conflicting reports about the effect of forearm position on spinal and cortical excitability of the elbow flexors, we examine the influence of contraction intensity. For the first time, excitability data are considered in a force steadiness context. Motoneuronal excitability is lowest in pronation and this disparity increases with contraction intensity. Cortical excitability exhibits a similar pattern from 5 to 25% of maximal force. Lower corticospinal excitability likely contributes to relatively poor force steadiness in pronation.

Keywords: biceps brachii, pronation, supination, transcranial magnetic stimulation, transmastoid stimulation

INTRODUCTION

Force (or torque) steadiness is an index of one’s ability to maintain muscle output at a desired level during an isometric contraction. It is quantified by the fluctuations in force (usually the coefficient of variation) about the mean value. Steadiness is influenced by contraction intensity (i.e., steadiness is lowest during very weak and very strong contractions; see Jakobi et al. 2018 for review) but can also be influenced by limb position. For example, elbow flexor steadiness is significantly lower with the forearm in a pronated (PRO) compared with neutral (NEU) or supinated (SUP) position (Brown et al. 2010; Smart et al. 2018). Maximal voluntary contraction (MVC) force is also lower in PRO compared with NEU and SUP (Kohn et al. 2018), and there is a strong negative relationship between coefficient of variation of force and MVC force (Brown et al. 2010). Brown and colleagues (2010) speculated that PRO was weakest (and least steady), in part, because of greater inhibition of biceps brachii motor units (Barry et al. 2008; ter haar Romeny et al. 1984). An influence of motoneuron pool output on steadiness is supported by evidence that the low-frequency component of motor unit discharge rates is largely responsible for explaining fluctuations in isometric force (Feeney et al. 2018; Negro et al. 2009). However, motoneuronal excitability has not yet been systematically investigated in the context of positional variability in force steadiness.

Recent data lend some support to the proposition of Brown and colleagues (2010), as it was shown that forearm position influences spinal and cortical excitability to the biceps brachii (Forman et al. 2016; Nuzzo et al. 2016). With the muscle relaxed, Nuzzo and colleagues (2016) found that motoneuronal excitability, as measured by the cervicomedullary motor-evoked potential (CMEP), was lower in PRO and NEU compared with SUP. Cortical excitability, as measured by the motor-evoked potential (MEP) normalized to the CMEP, was not different among the forearm positions. In contrast, Forman and colleagues (2016) observed a smaller MEP in PRO than NEU during a weak tonic contraction. Although the MEP was not normalized to the CMEP, CMEP size was not statistically different in PRO and NEU; hence, it was proposed that supraspinal mechanisms are primarily responsible for the influence of forearm position on MEP size (Forman et al. 2016). These seemingly conflicting results obtained from a relaxed versus contracting muscle indicate that neural drive is likely to play an important role in the forearm position-dependent effects on corticospinal excitability to biceps brachii and possibly force steadiness of the elbow flexors.

Irrespective of limb position, the amount of descending drive to a muscle undoubtedly has a profound influence on corticospinal excitability. Both MEPs (e.g., Hess et al. 1987; Martin et al. 2006; McNeil et al. 2011; Taylor et al. 1997) and CMEPs (McNeil et al. 2011) show a large increase from relaxation to contraction. In each case, the increase in size of the evoked potential is ascribed primarily to enhanced motoneuronal excitability (e.g., Di Lazzaro et al. 1998; Hess et al. 1987; Taylor et al. 1997). However, enhanced cortical excitability also contributes to the growth of the MEP (e.g., Di Lazzaro et al. 1998; Hess et al. 1987; Mazzocchio et al. 1994).

The aim of the present study was to extend recent investigations of the effect of forearm position on corticospinal excitability to biceps brachii (Forman et al. 2016; Nuzzo et al. 2016) and possibly reconcile differences between these studies by assessing the influence of neural drive (i.e., contraction intensity). Furthermore, we used a force steadiness task to assess the possible influences of spinal and cortical excitability on impaired steadiness in PRO compared with NEU and SUP (Brown et al. 2010). Force steadiness has critical consequences in the context of aging, stroke, and multiple sclerosis; therefore, it is a key factor for independent living (Oomen and van Dieën 2017) and targeting loci that might contribute to inefficient task performance is of great interest. It was hypothesized that both spinal and cortical excitability would be lower in PRO compared with NEU and SUP, with no difference between the latter two positions. The disparity for cortical and spinal excitability between PRO and NEU or SUP was expected to increase with contraction intensity.

METHODS

Participants.

In response to an advertisement posted across the university campus, 16 men volunteered for this study. All participants were healthy and showed no indication of neuromuscular or cardiovascular pathologies and had no contraindications (see Rossi et al. 2009) to transcranial magnetic stimulation (TMS). Each volunteer gave written informed consent and completed a TMS screening questionnaire before testing and all experimental procedures were approved by the institutional ethics committee. The experimental protocol consisted of one visit ~2 h in duration, and participants were asked to refrain from intense exercise and caffeine consumption 12 h before testing. Of the 16 volunteers, 1 discontinued the study due to nausea induced by TMS and 2 discontinued due to discomfort from transmastoid stimulation. Hence, the reported data were collected from 13 participants (26 ± 7 yr, means ± SD).

Participant setup.

Volunteers were seated in a custom-designed chair equipped with a linear calibrated force transducer (MLP-150; Transducer Techniques, Temecula, CA) set beneath a freely rotating handle and grounded via the Coulbourn Instruments Unit (Coulbourn Electronics, Allentown, PA). As previously described (Harwood et al. 2010; Fig. 1), the right arm was oriented with the shoulder at 10° abduction, 10° flexion, and the elbow at 90° flexion with the forearm supported on a foam brace. The rotating handle was positioned for the participant to grasp and rotate their forearm into the three isometric positions: SUP, NEU, and PRO. Real-time visual feedback was provided by a flat-screen monitor (20.5 in. at a distance of 1 m).

Fig. 1.

Fig. 1.

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Participant setup.

Electromyographic activity (EMG) was recorded from the biceps brachii using a monopolar electrode arrangement (4-mm rectangular Ag-AgCl; Kendall H59P electrodes; Covidien, Mansfield, MA) with the recording electrode over the muscle belly and the reference electrode at the distal tendon, grounded at the lateral epicondyle of the humerus. Force and EMG signals were sampled at 2,000 Hz, respectively, and recorded online using a 16-bit A/D converter (CED Power 1401-3; Cambridge Electronic Design) and Spike2 software (version 7.10; Cambridge Electronic Design). EMG signals were amplified (×100) and bandpass filtered (13–1,000 Hz) (Coulbourn Electronics).

Brachial plexus stimulation.

To assess the possible influence of forearm position on the compound muscle action potential (M-wave), a constant current stimulator (DS7AH; Digitimer, Welwyn Garden City, UK) delivered a single electrical stimulus (pulse duration of 200 μs, continuously variable voltage of ≤400 V) to the brachial plexus at Erb’s point. The cathode and anode were, respectively, located over the supraclavicular fossa and acromion with adhesive Ag-AgCl electrodes (10-mm diameter; Cleartrace; Conmed, Utica, NY). To obtain a maximal M wave (Mmax), the constant current output ranged from 48 to 132 mA.

Cervicomedullary stimulation.

Motoneuronal excitability was assessed with another DS7AH stimulator, which was used to pass a brief electric pulse (200 μs, ≤400 V) between Ag-AgCl electrodes (Cleartrace) fixed to the skin ~1- to 2-cm superior and medial to the mastoid processes (Gandevia et al. 1999; Ugawa et al. 1991). Stimulation intensity (110–215 mA) was set to evoke a CMEP of ~15% Mmax during a brief (~2 s) contraction at 5% MVC force, with the forearm in the NEU position.

Transcranial magnetic stimulation.

With the use of a Magstim 2002 stimulator (Magstim, Whitland, UK), the motor cortex was activated via a circular coil (13.5-cm outside diameter) held over the vertex of the head. The coil was oriented to preferentially activate the left hemisphere of the primary motor cortex. Stimulation intensity (44–100% of stimulator output) was set to elicit an MEP that matched the CMEP amplitude (~15% of Mmax) during a brief (~2 s) contraction at 5% MVC force in the NEU position.

Experimental procedures.

Data collection began with the determination of biceps brachii Mmax in the NEU position. With the participant relaxed, stimulus current was incrementally increased for successive stimuli until the peak-to-peak amplitude of Mmax plateaued; the intensity was further increased by 20%, and an additional three stimuli were delivered.

Following this, peak force for NEU was established by the performance of two or three brief (~2 s) MVCs, separated by ≥90 s of rest. Strong verbal encouragement and visual feedback of force were provided during all MVCs. Next, a target line was set at 5% MVC force and three Mmax responses were recorded during brief contractions at this intensity. TMS and cervicomedullary stimulation (CMS) intensities were separately established during brief contractions at 5% MVC force to elicit an MEP or CMEP, respectively, with an amplitude of ~15% Mmax. After the determination of stimulus intensities, the forearm position was changed to SUP or PRO (selected at random), and participants performed two or three brief MVCs and Mmax was collected at 5% MVC force. These steps were then repeated for the final position. As the current required to elicit Mmax was not necessarily the same for each position, 120% of the highest current was used for the remainder of the experiment.

The main protocol consisted of three blocks of contractions such that each forearm position was tested separately. The order of positions was prerandomized across participants so that there was an approximately even distribution of the possible combinations. Within each block, participants performed 24 brief (~6 s) isometric elbow flexion contractions. These contractions were grouped into six sets of four contractions, prerandomized among 5, 10, 25, and 50% MVC force. Half of the six sets involved TMS, and the other half involved CMS, which means that three MEPs and three CMEPs were collected at each contraction intensity. The order of sets within each block was prerandomized and the same for all participants. Twenty seconds of rest were provided between contractions, with no additional break between sets. During each contraction, participants were instructed to ramp their force to a preset submaximal target line and sustain their force as steadily as possible. After the target line was reached, a stimulus trigger was delivered to deploy either TMS or CMS 4.5 s later. Raw traces of the three MEPs and three CMEPs collected at 25% MVC force are shown for a single participant in Fig. 2. At the conclusion of a block, following a 2-min break, MVC force and Mmax (during 3 contractions at 5% MVC) were reassessed for that position. An additional 2-min rest was given at the conclusion of the postblock measures, and the participant’s forearm was rotated to the next position.

Fig. 2.

Fig. 2.

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Individual, overlaid traces of 3 cervicomedullary motor-evoked potentials (CMEPs) and 3 motor-evoked potentials (MEPs) recorded from a single participant at 25% maximal voluntary contraction force for all 3 forearm positions.

Data analysis.

Signal software (v. 5.08; Cambridge Electronic Design) was used offline to analyze all outcome variables, except force steadiness, which was analyzed with Spike2 software (v. 7.10; Cambridge Electronic Design). Data analyzed in Signal included the following: MVC force; CMEP, MEP, and Mmax peak-to-peak amplitude; and voluntary root mean square (RMS) EMG. MVC force was calculated as the peak value, whereas voluntary RMS EMG was calculated over the 150 ms before all stimuli and normalized to the control Mmax amplitude for that position. For each forearm position, within a contraction intensity, spinal excitability was calculated as the average absolute CMEP amplitude divided by the control Mmax amplitude (e.g., Gandevia et al. 1999). Cortical excitability was calculated as the average absolute MEP amplitude divided by the average absolute CMEP amplitude (e.g., Gandevia et al. 1999). Force steadiness (calculated across a 3-s period before the delivery of TMS or CMS) was measured as the coefficient of variation of force, determined by dividing the standard deviation of the force by the mean. A potential impairment to peripheral excitability (Mmax) or maximal force (MVC) was assessed for each position by normalizing the values obtained at the end of each block to those obtained before the start of the protocol.

Statistics.

All statistical analyses were completed with IBM SPSS Statistics (version 22.0; SPSS, Chicago, IL). An intraclass correlation (ICC) was applied to absolute amplitude measures for MEPs and CMEPs at 5% MVC for all forearm positions (3 measures per position per response type). Paired samples t tests were used to compare preprotocol MVC force and Mmax amplitude among forearm positions. Two-way repeated measures ANOVAs were run to test within-subject effects of position (PRO, NEU, and SUP) and contraction intensity (5, 10, 25, and 50% MVC) for the following variables: normalized prestimulus RMS EMG; force steadiness; normalized CMEP amplitude, and normalized MEP amplitude. Sphericity of data for each ANOVA was verified using Mauchly’s test, and, when needed, Greenhouse-Geisser corrections were applied. The effects of forearm position, contraction intensity, or significant interactions were followed up with paired samples t tests, as necessary. To fully address our aim to examine the influence of contraction intensity on the effect of forearm position on spinal and supraspinal excitability, we made the a priori decision to compare normalized CMEPs and MEPs among forearm positions. Consequently, normalized MEP amplitude was compared among positions with paired samples t tests despite the absence of a significant main effect of position or position × contraction intensity interaction.

To determine whether a block of contractions led to an impairment of maximal force production or an alteration of peripheral excitability for each forearm position, a two-way repeated measures ANOVA was run to assess within-subject effects of time (pre- and postprotocol values) and position (PRO, NEU, and SUP) of MVC force and Mmax amplitude. Significance for all data was defined as P < 0.05, with the exception of conditions requiring multiple comparisons; P < 0.017, when comparing the three positions at one contraction intensity and P < 0.008, when comparing the four contraction intensities within one position. Data are presented in text and in figures as the mean value ± standard deviation (SD).

RESULTS

Maximal force and force steadiness.

Absolute MVC force was greater in NEU (287 ± 59 N) compared with both SUP (249 ± 66 N) and PRO (152 ± 39N), with SUP greater than PRO (all P ≤ 0.001). To control for these differences in absolute force when testing for the development of fatigue, postprotocol MVC force in each position was expressed as a percentage of the baseline value (95.8 ± 4.7, 97.6 ± 6.2, and 105.7 ± 18.4% of baseline for NEU, SUP, and PRO, respectively). Analysis of these normalized forces gave no main effect of position (P = 0.082) or time (P = 0.904) and no interaction (P = 0.082), indicating no fatigue development.

A two-way repeated measures ANOVA for force steadiness (Fig. 3 and Supplemental Figure S1; all Supplemental Materials are available at: https://figshare.com/articles/Supplemental_Materials/10370033) gave main effects of position (P < 0.001) and contraction intensity (P < 0.001), as well as an interaction for position and contraction intensity (P < 0.001). At each contraction intensity, PRO was less steady than NEU and SUP (P ≤ 0.001), with no difference between the latter two positions (P ≥ 0.382). For both NEU and PRO, 5% MVC force was less steady than 10, 25, and 50% MVC (P < 0.001), with no differences among the other intensities (P ≥ 0.052). For SUP, 5% MVC force was less steady (P < 0.001) than 25 and 50% MVC but not different to 10% MVC (P = 0.090), and there were no differences among 10, 25, and 50% MVC (P ≥ 0.310).

Fig. 3.

Fig. 3.

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Force steadiness for 3 forearm positions and four contraction intensities. Mean values from 13 participants (±SD). Pronated (PRO) was less steady than neutral (NEU) and supinated (SUP) (*P < 0.05) at each contraction intensity. For PRO and NEU, steadiness was lower at 5% maximal voluntary contraction (MVC) than all other contraction intensities (†P < 0.05). For SUP, 5% MVC was less steady than 25 and 50% MVC (‡P < 0.05).

Compound muscle action potential and voluntary electromyography.

With correction for multiple comparisons, the paired samples t tests indicated that baseline Mmax amplitude was equivalent for NEU and SUP (6.22 ± 1.91 mV and 6.74 ± 1.95 mV, respectively; P = 0.035) and the amplitude for PRO (5.60 ± 1.81 mV) was smaller than both NEU (P < 0.001) and SUP (P = 0.002). To control for these differences when testing if peripheral excitability was altered by the contractions within a block, postprotocol Mmax amplitude in each position was expressed as a percentage of the baseline value (102.6 ± 17.1, 105.1 ± 13.8, and 102.5 ± 5.1% of baseline for NEU, SUP, and PRO, respectively). Analysis of these normalized values gave no main effect of position (P = 0.761) or time (P = 0.081) and no interaction (P = 0.761), indicating peripheral excitability was not altered by the protocol.

Prestimulus RMS EMG, normalized to Mmax at 5% MVC (Fig. 4 and Supplemental Figure S2; see https://figshare.com/articles/Supplemental_Materials/10370033), had main effects of position and contraction intensity (P < 0.001) as well as an interaction between the two variables (P < 0.001). At 5% MVC force, PRO had a higher normalized RMS EMG than NEU and SUP (P ≤ 0.005), with no difference between NEU and SUP (P = 0.064). At 10% MVC force, there were no differences in normalized RMS EMG among positions (P ≥ 0.084). At 25 and 50% MVC force, PRO was less than both NEU and SUP (P ≤ 0.006), with no difference between NEU and SUP (P ≥ 0.072). As expected, normalized RMS EMG increased with contraction intensity for all positions (P < 0.001).

Fig. 4.

Fig. 4.

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Root mean square (RMS) EMG of the biceps brachii as a percentage of maximal M wave (Mmax) recorded at 5% maximal voluntary contraction (MVC) force. Mean values are from 13 participants (±SD). Pronated (PRO) was statistically greater compared with supinated (SUP) and neutral (NEU) at 5% MVC force but statistically lower at 25 and 50% MVC force (†P < 0.017). For all positions, RMS EMG increased with contraction intensity (*P < 0.05).

Spinal and supraspinal excitability.

Absolute amplitudes for MEPs and CMEPs had an average ICC measure of 0.841 and 0.816, respectively, indicating good reliability. Spinal excitability, characterized by normalized CMEP amplitude (Fig. 5A and Supplemental Figure S3A; see https://figshare.com/articles/Supplemental_Materials/10370033), had a main effect of position (P < 0.001) and contraction intensity (P < 0.001) and an interaction between position and intensity (P = 0.011). When the effect of position at each contraction intensity was examined, paired samples t tests (using a Bonferroni corrected value of P < 0.017 to reflect three comparisons) showed an increase in spinal excitability for SUP compared with PRO at all contraction intensities (P ≤ 0.004) and for NEU compared with PRO at 25 and 50% MVC (P ≤ 0.010). There was no difference between NEU and SUP at any contraction intensity (P ≥ 0.042). When examining the effect of contraction intensity within each position, paired samples t tests (using a Bonferroni corrected value of P < 0.008 to reflect six comparisons) showed a progressive increase of spinal excitability with increasing contraction intensity in all positions (P ≤ 0.002), with the exception of no difference between 5 and 10% MVC (P ≥ 0.018).

Fig. 5.

Fig. 5.

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Normalized cervicomedullary motor-evoked potential (CMEP) and motor-evoked potential (MEP) amplitudes for 3 forearm positions and 4 contraction intensities. Mean values from 13 participants (±SD). A: spinal excitability was lower for pronated (PRO) compared with neutral (NEU) and supinated (SUP) (†P < 0.05). In each position, excitability increased with contraction intensity after 10% maximal voluntary contraction (MVC) (*P < 0.05). B: cortical excitability was not different among positions (P = 0.055); however, an a priori post hoc showed PRO had reduced excitability than NEU at 25% MVC (*P = 0.006) with no difference between NEU and SUP (P = 0.085).

Cortical excitability, measured by normalized MEP amplitude (Fig. 5B and Supplemental Figure S3B; see https://figshare.com/articles/Supplemental_Materials/10370033), had no effect of position (P = 0.055), a main effect of contraction intensity (P = 0.010), and no interaction (P = 0.104). A Bonferroni corrected pairwise comparison of intensity, collapsed across position, revealed a larger MEP at 25% compared with 5% (P = 0.001) and 10% (P = 0.006), with no difference for 25% MVC compared with 50% MVC (P = 0.146). An a priori paired samples t test for comparison among positions (Bonferroni corrected P = 0.008) within a contraction intensity revealed a 39.8 ± 38.3% lower amplitude for PRO compared with NEU at 25% MVC force (P = 0.006), with no difference between NEU and SUP (P = 0.085) or between SUP and PRO (P = 0.048). All other contraction intensities were not statistically different among positions (P ≥ 0.110).

DISCUSSION

As expected, force steadiness of the elbow flexors was lower in PRO than NEU and SUP. Furthermore, as hypothesized, spinal motoneuronal excitability was lower in PRO compared with NEU and SUP, highlighting that forearm position has a comparable impact on both force steadiness and motoneuronal excitability. While cortical excitability did not have a main effect for position, an a priori assessment indicated that it was lower for PRO than NEU at 25% MVC force. Our data, collected at a variety of contraction intensities, support elements of two recent studies that report seemingly conflicting findings (Forman et al. 2016; Nuzzo et al. 2016) and help to explain the discrepancies between the two. The observed reductions in spinal and cortical excitability in PRO likely contribute to the reduced force steadiness and MVC force in this position (e.g., Brown et al. 2010; Smart et al. 2018).

Spinal excitability.

Similar to Nuzzo and colleagues (2016), we observed reduced motoneuronal excitability for PRO compared with NEU and SUP. Forman and colleagues (2016) did not test the SUP position but reported that motoneuronal excitability was not different between PRO than NEU during a weak tonic contraction, a result supported by the present data at 5 and 10% MVC force. As seen in Fig. 5A, the increase of the CMEP with contraction intensity was blunted for PRO compared with NEU and SUP. Consequently, the effect of forearm position on motoneuronal excitability was magnified with increasing contraction intensity. Irrespective of the mechanism(s) involved, this finding emphasizes the importance of considering contraction intensity when investigating different forearm positions.

It is likely that afferent feedback plays a key role in the lower spinal excitability for PRO compared with NEU and SUP (Barry et al. 2008; Gerilovsky et al. 1989; Ginanneschi et al. 2005; Forman et al. 2016; Hwang 2002). A recent study showed that sophisticated control laws exist at a spinal level for limb perturbation during a target-reaching task (Weiler et al. 2018). The stretch reflex was dependent not only on the position of the wrist and elbow, but also the position of the forearm, such that the reflex was inverted in an upright compared with flipped hand position (i.e., SUP vs. PRO). Weiler and colleagues speculated that the underlying mechanism for their observations might involve GABAergic spinal interneuron recruitment, like those observed to modulate the gain of sensory feedback in mice (Fink et al. 2014). Furthermore, Yaguchi and colleagues (2015) have shown that spinalization at C2 in male rhesus macaques does not eliminate the position-dependent responses evoked by intraspinal microstimulation. These results suggest forearm posture plays a key role in modulating descending cortical drive via a spinally mediated “posture-dependent filter” (Yaguchi et al. 2015).

Motor unit properties, including motor unit force and discharge rate variability, are impacted by forearm position (Enoka et al. 2003; Harwood et al. 2010), such that force steadiness is reduced with increased discharge rate variability (Harwood et al. 2010). It follows that the spinal processes that influence motoneuronal excitability (and its reduction in PRO) will also contribute to the concurrent observation of reduced force steadiness in PRO. Motor unit data from Negro and colleagues (2009) provide evidence that 74% of the variability in force steadiness can be explained by the common synaptic input to motoneurons (Feeney et al. 2018). The exact mechanism for reduced steadiness in PRO is unclear; however, it likely involves contribution from afferent feedback and descending drive, both of which are modulated by forearm position.

Cortical excitability.

Our finding of lower cortical excitability for PRO than NEU at 25% MVC force (Fig. 5B) supports the suggestion of Forman and colleagues (2016) that supraspinal mechanisms contributed to their observation of a smaller MEP for PRO than NEU during a weak tonic contraction. Nuzzo and colleagues (2016) found no effect of forearm position on the MEP (normalized to CMEP) recorded from a relaxed muscle, but, again, this fits with our observations with minimal muscle activation (5% MVC). Similar to the CMEP data, the influence of forearm position on the normalized MEP is dependent on the contraction intensity; however, the pattern is rather different beyond 25% MVC force. Between 5 and 25% MVC force, the relationship for each position was comparable to that seen for motoneuronal excitability; i.e., a nearly linear increase of cortical excitability with contraction intensity that was blunted for PRO compared with NEU and SUP. Between 25 and 50% MVC force, PRO continued to follow a linear increase whereas SUP was unchanged and NEU decreased considerably, such that the normalized MEP for all positions converged at the same point. We are not aware of another study to assess the influence of contraction intensity on biceps brachii MEPs and CMEPs for PRO or NEU, but our SUP data fit with previous findings. Taylor and colleagues (2002) reported an increase in cortical excitability from relaxation to 20% MVC torque, whereas Martin and colleagues (2006) reported no change in cortical excitability from 50 to 100% MVC torque. With reduced neural drive for PRO compared with SUP (Fig. 4; Kohn et al. 2018), it is sensible that cortical excitability would increase to a higher percentage of maximal force in PRO.

Potential mechanisms for a smaller MEP in PRO compared with NEU or SUP have been described by others (Forman et al. 2016; Nuzzo et al. 2016; Perez and Rothwell 2015). These authors largely agree that afferent feedback, which is influenced by forearm position, plays some role in modulating cortical excitability, such that intracortical facilitation impacts the evoked response magnitude. Reduced intracortical facilitation for PRO, further mediated by a potential “posture-dependent filter” at a spinal level (Yaguchi et al. 2015), would likely contribute to reduced force steadiness for PRO. The influence of this facilitation appears to increase with contraction intensity, as shown by the main effect of intensity on MEP amplitude. Furthermore, the greater MEP for NEU than PRO at 25% MVC force suggests that the forearm-position influence on afferent feedback also increases with contraction intensity. Although there is no experimental evidence to support the hypothesis, it is possible that a feedforward mechanism may exist for this task, which provides the sensorimotor system access to predictive arm dynamics for a prespecified forearm position in preparation of an isometric contraction (Davidson and Wolpert 2005).

Voluntary electromyography.

The normalized RMS EMG of biceps brachii largely paralleled our force steadiness data and was comparable for NEU and SUP at all contraction intensities, with both positions greater than PRO, albeit only at 25 and 50% MVC force (see also Harwood et al. 2010; Jamison and Caldwell 1993). Interestingly, at 5% MVC force, normalized RMS EMG was greater for PRO compared with NEU and SUP. Although these data are statistically significant, given that the disparity in force steadiness between PRO and the other positions is greatest at 5% MVC force, they are unlikely to have a physiological significance. The increase in RMS EMG with contraction intensity is rather modest for PRO and could be caused by several mechanisms. One possible mechanism is higher biceps brachii motor unit recruitment thresholds for PRO compared with SUP (ter haar Romeny et al. 1982, 1984; van Zuylen et al. 1988). To this end, two studies found that some motor units active in NEU and SUP were not recruited in PRO at 10% (Harwood et al. 2010) or 50% MVC force (ter haar Romeny et al. 1984), which would reduce both EMG activity and maximal force. Another potential mechanism is lower descending drive. It was reported recently (Kohn et al. 2018) that PRO not only had a lower maximal force but also lower voluntary activation (70.9 ± 20.4%) compared with NEU and SUP (96.1 ± 3.2% and 93.0 ± 5.2%, respectively). Finally, the lower biceps brachii EMG (beyond 10% MVC force) and elbow flexor force in PRO compared with NEU or SUP, could relate to reciprocal inhibition between the biceps brachii and other arm muscles, such as the triceps brachii (Katz et al. 1991), brachioradialis (Barry et al. 2008; Miyasaka et al. 2007; Naito et al. 1996), and pronator teres (Naito et al. 1998). This inhibition has been noted to progressively increase as the forearm moves from SUP to PRO, and is further strengthened by coupling PRO with a low level of EMG activity (Barry et al. 2008).

Compound muscle action potential.

In the present study, the Mmax collected at 5% MVC force was larger for SUP (and NEU) compared with PRO. Nuzzo and colleagues (2016) found that the Mmax recorded from relaxed muscle was smaller for SUP compared with NEU or PRO and attributed the difference to the spatial arrangement of muscle fibers beneath the recording electrodes. This discrepancy of relative Mmax size across forearm positions for weakly contracting versus relaxed muscle is curious and could be the result of different electrode positioning in the two studies. Regardless, because Mmax size is influenced by forearm position, this measure should be monitored to ensure proper interpretation of CMEPs or MEPs.

Conclusion.

We have shown that motoneuronal excitability is inhibited/disfacilitated in PRO compared with NEU and SUP, with cortical excitability exhibiting a similar pattern from 5 to 25% MVC. This is likely mediated at a spinal level by afferent feedback, which may impact the magnitude of reciprocal inhibition and biceps brachii motor unit recruitment thresholds. Cortical effects may reflect afferent feedback and feedforward mechanisms, but further study is required for elucidation. The electrophysiology data support both previous and present observations of reduced force steadiness in PRO, as increasing levels of spinal and cortical excitability (i.e., greater descending drive and, therefore, voluntary activation) are linked to higher force steadiness (Kohn et al. 2018). Notably, the magnitude of the disparity between PRO and NEU or SUP was influenced by contraction intensity, so it is important to consider the level of neural drive when examining the influence of forearm position on corticospinal excitability and force steadiness.

GRANTS

This work was supported by Gouvernement du Canada/Natural Sciences and Engineering Research Council of Canada (Conseil de Recherches en Sciences Naturelles et en Génie du Canada) Grant 435912-2013 (to C. J. McNeil); Canada Foundation for Innovation/British Columbia Knowledge Development Fund Grant 32260 (to C. J. McNeil); and Gouvernement du Canada/Natural Sciences and Engineering Research Council of Canada (Conseil de Recherches en Sciences Naturelles et en Génie du Canada) Grant 312038-2017 (to J. M Jakobi).

DISCLOSURES

No conflicts of interest, financial or otherwise, are declared by the authors.

AUTHOR CONTRIBUTIONS

A.F.Y., J.M.J., and C.J.M. conceived and designed research; A.F.Y. and S.L.K. performed experiments; A.F.Y. and S.L.K. analyzed data; A.F.Y., J.M.J., and C.J.M. interpreted results of experiments; A.F.Y. prepared figures; A.F.Y. drafted manuscript; A.F.Y., J.M.J., and C.J.M. edited and revised manuscript; A.F.Y., S.L.K., J.M.J., and C.J.M. approved final version of manuscript.

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