Use-dependent corticospinal excitability is associated with resilience and physical performance during simulated military operational stress

Abstract

Simulated military operational stress (SMOS) provides a useful model to better understand resilience in humans as the stress associated with caloric restriction, sleep deficits, and fatiguing exertion degrades physical and cognitive performance. Habitual physical activity may confer resilience against these stressors by promoting favorable use-dependent neuroplasticity, but it is unclear how physical activity, resilience, and corticospinal excitability (CSE) relate during SMOS. To examine associations between corticospinal excitability, physical activity, and physical performance during SMOS. Fifty-three service members (age: 26 ± 5 yr, 13 women) completed a 5-day and -night intervention composed of familiarization, baseline, SMOS (2 nights/days), and recovery days. During SMOS, participants performed rigorous physical and cognitive activities while receiving half of normal sleep (two 2-h blocks) and caloric requirements. Lower and upper limb CSE were determined with transcranial magnetic stimulation (TMS) stimulus-response curves. Self-reported resilience, physical activity, military-specific physical performance (TMT), and endocrine factors were compared in individuals with high (HIGH) and low CSE based on a median split of lower limb CSE at baseline. HIGH had greater physical activity and better TMT performance throughout SMOS. Both groups maintained physical performance despite substantial psychophysiological stress. Physical activity, resilience, and TMT performance were directly associated with lower limb CSE. Individual differences in physical activity coincide with lower (but not upper) limb CSE. Such use-dependent corticospinal excitability directly relates to resilience and physical performance during SMOS. Future studies may use noninvasive neuromodulation to clarify the interplay among CSE, physical activity, and resilience and improve physical and cognitive performance.NEW & NOTEWORTHY We demonstrate that individual differences in physical activity levels coincide with lower limb corticospinal excitability. Such use-dependent corticospinal excitability directly relates to resilience and physical performance during a 5-day simulation of military operational stress with caloric restriction, sleep restriction and disruption, and heavy physical and cognitive exertion.

Keywords: motor cortex; physical activity; resilience; transcranial magnetic stimulation; use-dependent plasticity.

Graphical abstract

Figure 1.

Experimental procedures. A: all participants completed five consecutive days of simulated military operational stress (SMOS). Participants were familiarized with the study procedures (Day 0) and then completed baseline testing (Day 1), 2 days of SMOS (Days 2 and 3), and a recovery day (Day 4). Every morning, we assessed mood. Throughout SMOS, we assessed physical performance, endocrine factors, and corticospinal excitability. B: during each day of SMOS, participants received 50% of their total energy expenditure estimate and 4 h sleep (in two 2-h blocks). During baseline and recovery testing, participants received 8 h sleep and individualized meals to meet their estimated total daily energy expenditure requirement. Caloric intake on Day 4 does not reflect total daily energy expenditure (participants discharged in the late afternoon). Solid lines show time asleep, dashed lines show caloric intake; N = 53. Data are means ± SD. No statistical analysis was performed; descriptive statistics only.

Figure 2.

Experimental protocol to derive corticospinal excitability stimulus-response curves and median split. A: corticospinal excitability was assessed in the dominant first dorsal interosseus and vastus lateralis in n = 53 individuals following a series of maximum voluntary contractions (MVCs). B: for each muscle, a total of 40 pulses were delivered during eight 25 s sets of isometric contractions at 15%MVCs, with five pulses applied at random 5% increments of stimulator output (range: 5%–100%) per set. C: representative motor-evoked potentials (MEPs) at select percentages of stimulator output were (D and E) fitted to a Boltzmann sigmoidal curve to derive muscle-specific stimulus-response-curves for each day. Corticospinal excitability was then determined as the plateau (MEP_MAX) of the stimulus-response-curve. F: neither lower nor upper limb corticospinal excitability changed throughout the intervention, but a persistent bimodal distribution of lower limb MEPs was evident. As a result, we divided the sample into individuals with HIGH (n = 27) and LOW (n = 26) corticospinal excitability of the VL using a median split of baseline (Day 1) MEP_MAX.

Figure 3.

Lower and upper limb corticospinal excitability during simulated military operational stress. A and B: lower (but not upper) limb corticospinal excitability was greater in HIGH (n = 26; blue) than LOW (n = 27; yellow), but neither were affected by simulated military operational stress overall. Data were logarithmically transformed and analyzed using a three-way repeated-measures ANCOVA (2 groups × 2 muscles × 4 days; covariate = body fat percentage). Asterisks (*) and vertical bars indicate a main effect of group (P < 0.05). Gray-shaded areas indicate the timing of the intervention. Data are means ± SD. FDI, first dorsal interosseous; MEP, motor-evoked potential; VL, vastus lateralis.

Figure 4.

Physical activity profile of individuals with high (HIGH) and low (LOW) corticospinal excitability. A: weekly time spent physically active differed between activity types, with weight training, walking, loaded walking, and running most frequently reported. B: LOW reported lower levels of physical activity, and this difference persisted after activity-specific differences in metabolic equivalents were considered (C). D: the relative contribution of each activity type to weekly physical activity did not differ. Boxplots in A demonstrate the median, 25th, and 75th percentile. Stacked bar charts in B and D show the mean physical activity and percentage contribution per activity type, respectively. Raincloud plot in C demonstrates the probability density distribution, boxplot, and individual datapoints for group-specific metabolic equivalent (MET) minutes per week. HIGH (n = 25) is shown in blue, whereas LOW (n = 27) in yellow in C. Data were compared using an independent t test (C) or a mixed-model ANOVA (2 groups × 13 physical activity subtypes). MMA, mixed-martial-arts. Asterisk (*) indicates significant main effect of physical activity type (A) and group (B) or a significant between-group difference (C).

Figure 5.

Influence of simulated military operational stress on mood, military-specific physical performance, strength, and endocrine factors. A: mood (n = 53) worsened throughout simulated military operational stress (SMOS). B: HIGH performed better on the physical performance tests (TMT, n = 39), despite similar maximal isometric strength in the FDI (D) and VL (C) (n = 46). Neither strength nor physical performance declined during SMOS. E: nevertheless, canonical exercise-induced endocrine responses were evident from pre- to post-TMT Data were analyzed using a repeated-measures ANOVA with one between-group factor (2 groups) and one (3- or 4 days; mood, TMT, strength) or two (3- or 4 days × 2 timepoints; cortisol, IGF-I, BDNF, GH) within-group factors. GH and BDNF were log-transformed before analysis. The gray-shaded areas correspond to the SMOS intervention. HIGH (n = 26) are shown in blue, whereas LOW (n = 27) are shown in yellow. Asterisks (*) and horizontal/vertical bars indicate a main effect of day/group, whereas asterisks and brackets ( [ ) indicate main effects of time (pre- to post-TMT). Hashtags (#) indicate significant pairwise difference after Bonferroni correction. Data show means ± SD. For all tests P < 0.05. BDNF, brain-derived neurotrophic factor (n = 34), cortisol (n = 45); FDI, first dorsal interosseus; GH, growth hormone (n = 38); IGF-I, insulin-like growth factor I (n = 52); TMT, tactical mobility test; VL, vastus lateralis.

Figure 6.

Physical activity, resilience, performance, and corticospinal excitability. A–C: higher corticospinal excitability of the vastus lateralis (VL) was associated with greater physical activity (n = 52), resilience (n = 52), and tactical mobility test (TMT) performance (n = 49). Associations were examined using Pearson correlation. CD-RISC, Connor-Davidson Resilience Scale; FDI, first dorsal interosseous; MEP, motor-evoked potential; MET, metabolic equivalent. Negative scores on the TMT performance test indicate better performance.