Neuromuscular electrical stimulation training induces atypical adaptations of the human skeletal muscle phenotype: a functional and proteomic analysis

Abstract

The aim of the present study was to define the chronic effects of neuromuscular electrical stimulation (NMES) on the neuromuscular properties of human skeletal muscle. Eight young healthy male subjects were subjected to 25 sessions of isometric NMES of the quadriceps muscle over an 8-wk period. Needle biopsies were taken from the vastus lateralis muscle before and after training. The training status, myosin heavy chain (MHC) isoform distribution, and global protein pattern, as assessed by proteomic analysis, widely varied among subjects at baseline and prompted the identification of two subgroups: an "active" (ACT) group, which performed regular exercise and had a slower MHC profile, and a sedentary (SED) group, which did not perform any exercise and had a faster MHC profile. Maximum voluntary force and neural activation significantly increased after NMES in both groups (+∼30% and +∼10%, respectively). Both type 1 and 2 fibers showed significant muscle hypertrophy. After NMES, both groups showed a significant shift from MHC-2X toward MHC-2A and MHC-1, i.e., a fast-to-slow transition. Proteomic maps showing ∼500 spots were obtained before and after training in both groups. Differentially expressed proteins were identified and grouped into functional categories. The most relevant changes regarded 1) myofibrillar proteins, whose changes were consistent with a fast-to-slow phenotype shift and with a strengthening of the cytoskeleton; 2) energy production systems, whose changes indicated a glycolytic-to-oxidative shift in the metabolic profile; and 3) antioxidant defense systems, whose changes indicated an enhancement of intracellular defenses against reactive oxygen species. The adaptations in the protein pattern of the ACT and SED groups were different but were, in both groups, typical of both resistance (i.e., strength gains and hypertrophy) and endurance (i.e., a fast-to-slow shift in MHC and metabolic profile) training. These training-induced adaptations can be ascribed to the peculiar motor unit recruitment pattern associated with NMES.

Lack of functional effects of neuromuscular electrical stimulation on skeletal muscle oxidative metabolism in healthy humans

“…Together with the increased muscle force (12), an enhanced oxidative function in vivo could significantly increase the exercise tolerance of the treated subjects, and, if confirmed also in other populations, could make NMES well suited to treat conditions of disuse/immobilization, or other pathological conditions characterized by an impaired muscle function. Rather surprisingly, however, the hypothesis was not confirmed by the obtained results, which demonstrated no significant changes of the investigated variables.…”

“…The training program consisted of twenty-five 18-min sessions of isometric NMES of both quadriceps, carried out over 8 wk, with three sessions/wk. Details on the NMES protocol can be found in Gondin et al (12). The protocol had been successfully used in previous studies to increase knee extensor muscle strength (13).…”

“…In the light of these controversial results, Gondin et al (12) performed a comprehensive in vitro evaluation of the skeletal muscle phenotypic adaptations following a training program by NMES. These authors observed the following (12): increases in maximum voluntary force and neural activation; muscle fibers hypertrophy; a fast-to-slow transition of muscle fiber types, as determined on the basis of myosin heavy chain (MHC) isoforms; a fast-to-slow phenotype shift in the expression of myofibrillar proteins; a glycolytic-to-oxidative shift in metabolic profile; and an enhancement of intracellular defenses against reactive oxygen species.…”

“…These authors observed the following (12): increases in maximum voluntary force and neural activation; muscle fibers hypertrophy; a fast-to-slow transition of muscle fiber types, as determined on the basis of myosin heavy chain (MHC) isoforms; a fast-to-slow phenotype shift in the expression of myofibrillar proteins; a glycolytic-to-oxidative shift in metabolic profile; and an enhancement of intracellular defenses against reactive oxygen species. As discussed by the authors (12), these muscular adaptations could be attributed to the peculiar motor unit recruitment pattern associated with NMES (12,28) and appear of interest since they are typical of both resistance (strength gains and hypertrophy) and endurance (fast-to-slow shift in MHC and metabolic profile) training.…”

Electrical stimulation for neuromuscular testing and training: state-of-the art and unresolved issues

“…Future efforts should be directed at investigating more precisely the locus/loci of neural adaptations induced by NMES; in particular, supraspinal mechanisms/sites such as cortical excitability and cortical maps could be explored using transcranial magnetic stimulation and functional magnetic resonance imaging, techniques that are nowadays relatively accessible. The determinants of phenotypic variability in response to NMES strength training also require greater attention (Gondin et al 2011a), with particular emphasis on factors that should be controlled, such as training intensity. Once the physiological mechanisms underlying neural and/or muscular changes to NMES training are substantiated by research evidence, one or both forms of adaptation (or even specific mechanisms) could be specifically targeted according to the individual needs of the end user.…”