Neural determinants of the increase in muscle strength and force steadiness of the untrained limb following a 4-week unilateral training

Abstract

Enhanced untrained muscle strength and force steadiness following unilateral resistance training (i.e., cross-education) is typically attributed to neural responses. However, the mechanisms of these adaptations for spinal motoneurons remain unexplored. Therefore, we examined maximal-voluntary-force (MVF), steady-force variability (CovF), and longitudinally tracked motor unit adaptations in 10 individuals completing a 4-week unilateral strength intervention compared to 9 controls. High-density surface electromyography was recorded from the biceps brachii during steady (10%MVF) and trapezoidal (35%MVF) contractions. The relative proportion of common synaptic input (CSI) to motoneurons and its variability (CSI-V) were estimated using coherence and spectral analysis. Indirect estimates of persistent inward currents using firing rate hysteresis ({Delta}F) and motor unit recruitment thresholds (MURT) were assessed during the ramp forces (35%MVF). MVF increased in both the trained (+14%, p<0.001) and untrained limbs (+6%, p=0.004), and CovF decreased in both limbs (p<0.001). Greater CSI was observed on both sides (p<0.01), concomitant with reduced CSI-V (p<0.01). {Delta}F increased exclusively in the trained limbs (+1.61{+/-}0.71 pps; p<0.001), and both sides exhibited lower MURT (p<0.001). In trained limbs, MVF gains were strongly associated with changes in CSI, MURT, and {Delta}F (R{superscript 2}>0.70, p<0.01), while the contralateral muscle MVF increase was associated exclusively with CSI and MURT (R{superscript 2}>0.65, p<0.01). In both limbs, lower CovF was strongly associated with reduced CSI-V (R{superscript 2}>0.70, p<0.01). Our findings suggest that enhanced untrained muscle force and steadiness are mediated by increased relative strength of shared synaptic input with respect to independent noise and decreased variability of this shared input, with gains in trained muscle MVF being associated with {Delta}F. Key pointsO_LIUnilateral resistance training improves strength and force steadiness in the contralateral untrained limb, suggesting neural adaptations without directly overloading the muscle. C_LIO_LIDespite established force-related modifications, the specific neural mechanisms mediating these functional responses remain largely unknown. C_LIO_LI4-week unilateral training intervention enhanced muscle strength and force steadiness in the untrained limbs of 10 individuals, alongside a greater proportion of shared synaptic input, reduced variance in common input, and lower motor unit recruitment thresholds. C_LIO_LIWe demonstrate that the neural mechanisms underlying improved strength and force control in muscles without mechanical overloading are associated with a higher relative shared input among motoneurons and reduced variance in these common input components. C_LI O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=148 SRC="FIGDIR/small/645159v1_ufig1.gif" ALT="Figure 1"> View larger version (33K): org.highwire.dtl.DTLVardef@1a9e7feorg.highwire.dtl.DTLVardef@1bdd9a6org.highwire.dtl.DTLVardef@11c5ba0org.highwire.dtl.DTLVardef@c39a42_HPS_FORMAT_FIGEXP M_FIG O_FLOATNOC_FLOATNO unilateral training intervention reduced the variance in common synaptic input (CSI-V), which was associated with decreased variability in force steadiness (CovF) in both the trained and contralateral untrained limbs. On the exercised side, the increase in maximal voluntary force (MVF) was accompanied by a higher proportion of common synaptic input (CSI), a lower motor unit recruitment threshold (RT), enhanced persistent inward current (PIC) amplitude, and increased neural drive. In contrast, the contralateral untrained limb exhibited higher shared synaptic input and a lower RT but with unaltered PIC amplitude and neural drive ({leftrightharpoons}). Overall, these adaptations resulted in a 14% increase in MVF in the exercised limb and a 6% increase in the untrained limb. C_FIG