The knowns and unknowns of neural adaptations to resistance training

Abstract

The initial increases in force production with resistance training are thought to be primarily underpinned by neural adaptations. This notion is firmly supported by evidence displaying motor unit adaptations following resistance training; however, the precise locus of neural adaptation remains elusive. The purpose of this review is to clarify and critically discuss the literature concerning the site(s) of putative neural adaptations to short-term resistance training. The proliferation of studies employing non-invasive stimulation techniques to investigate evoked responses have yielded variable results, but generally support the notion that resistance training alters intracortical inhibition. Nevertheless, methodological inconsistencies and the limitations of techniques, e.g. limited relation to behavioural outcomes and the inability to measure volitional muscle activity, preclude firm conclusions. Much of the literature has focused on the corticospinal tract; however, preliminary research in non-human primates suggests reticulospinal tract is a potential substrate for neural adaptations to resistance training, though human data is lacking due to methodological constraints. Recent advances in technology have provided substantial evidence of adaptations within a large motor unit population following resistance training. However, their activity represents the transformation of afferent and efferent inputs, making it challenging to establish the source of adaptation. Whilst much has been learned about the nature of neural adaptations to resistance training, the puzzle remains to be solved. Additional analyses of motoneuron firing during different training regimes or coupling with other methodologies (e.g., electroencephalography) may facilitate the estimation of the site(s) of neural adaptations to resistance training in the future.

Keywords: Descending tracts; High-density surface electromyography; Motor cortex; Motor neuron; Strength; Synaptic input; Transcranial magnetic stimulation.

Fig. 1

Possible sites of neural adaptation to resistance training. Many potential sites of neural adaptations to resistance training have been suggested. Changes in intracortical inhibitory interneurons (IN; A) have been demonstrated following resistance training in both human (Weier et al. 2012) and non-human primates (Glover and Baker 2020). Adaptations within the corticospinal tract (CST), the main conduit of movement signals in humans, have been equivocal, but may occur at the level of the corticomotoneuronal synapse (B) or via corticospinal projections to interneurons (C) (Nuzzo et al. ; Colomer-Poveda et al. ; Siddique et al. 2020). Though human data is lacking, experiments in primates suggest contribution of the reticulospinal tract (RST), a bilateral descending tract implicated in gross motor tasks, to increased force production following resistance training (Glover and Baker 2020), which may occur via corticoreticular connections (D), reciprocal reticular connections (E), reticulospinal projections to interneurons (F), or monosynaptic reticular projections to motoneurons (α-MNs; G). The potential neural substrate for resistance training adaptations is also the increased monoaminergic drive via brainstem projections, increasing the strength of persistent inward currents within motoneurons and thus up-regulating depolarisation and shortening the afterhyperpolarisation phase of motoneurons (H and I). Electrophysiological adaptations are also possible within the motor units themselves (J) and might be particularly potent in high-threshold motor units (Casolo et al. 2019). Finally, adjustments in the sensory feedback from muscle via Ia afferent neurons may occur with resistance training (Aagaard et al. ; Durbaba et al. 2013) either through monosynaptic connections to motoneurons (K) or via spinal interneurons (L). Adapted from Glover and Baker (2020)

Fig. 2

The responses commonly used to assess the site of neural adaptation to resistance training. Early studies have shown increased responses to percutaneous mixed nerve stimulation during a contraction following resistance training (e.g., Sale et al. ; Aagaard et al. 2002)—these responses are known as the H-reflex (a), which is a long-latency response to submaximal nerve stimulation often evoked with a small M-wave (note the short-latency response), and the V-wave (b), which is a long-latency response to supramaximal nerve stimulation (hence the presence of a short-latency maximal M-wave; for further details on methodology see Burke and Gandevia 1999). In recent decades, transcranial magnetic stimulation (for details on methodology see Rossini et al. 2015) has been used to infer the site of neural adaptation to resistance training; however, the response to such stimuli, known as the motor evoked potentials followed by the silent period (c), have yielded variable results when assessed after resistance training (for meta-analysis see Siddique et al. 2020). Since responses to transcranial magnetic stimulation alone cannot differentiate between the cortical and spinal site of adaptation, additional methods have had to be employed, such as responses to direct activation of corticospinal axons, e.g., lumbar evoked potentials (d), but they have been shown not to change following resistance training (Nuzzo et al. ; Ansdell et al. 2020). It is important to note that changes in responses to stimulation techniques following resistance training are likely to be specific to the training task (Kalmar 2018)—as a result there have been recent attempts to replicate the training task when assessing responses to stimulation (E; from Brownstein et al. , with permission). Data displaying responses is from the personal archive of the authors—the average of 5 responses is displayed in colour with individual response overlaid in black

Fig. 3

Motor unit changes following strength training. a Whilst the more invasive fine-wire/needle electromyography is still considered the ‘gold standard’ for discerning the activity of single motor unit action potentials, recent advances in technology have allowed decomposition (line 1 in orange) of the interference electromyogram (the summated motor unit activity) from surface recordings (i.e., high-density EMG). Inferring changes in the nervous system from the global surface EMG is limited due to amplitude cancellation and the non-linear relationship between the size of action potentials and recruitment threshold; however, decomposition of the signal into individual motor unit spike trains infers activity of single motoneurons due to one-to-one relationship between axonal (left) and motor unit (right) action potentials by the muscle unit. From Del Vecchio et al. (2020), with permission. b A raster plot of decomposed motor unit spike trains from high-density EMG during a trapezoidal contraction at 35% of maximal force before and after short-term resistance training (intervention) or no change in physical activity (control). Short-term resistance training decreased motor unit recruitment thresholds (note the dark blue boxes), whereas derecruitment thresholds remained unchanged. Adapted from Del Vecchio et al. (2019), with permission. c Concomitantly with decreased recruitment thresholds, motor unit firing rate have also been shown to be augmented with short-term resistance training when the same motor units are tracked across time (Del Vecchio et al. 2019), whereas no such phenomenon is observed in the control group; consistent with the data previously obtained from fine-wire electromyography (Van Cutsem et al. 1998). The scatter plot and data from Del Vecchio et al. (2019), with permission