Psychosocial stress alters the strength of reticulospinal input to the human upper trapezius

Abstract

Psychosocial stress has been shown to influence several aspects of human motor control associated with the fight-or-flight response, including augmentation of upper trapezius muscle activity. Given the established role of the reticular formation in arousal, this study investigated the contribution of reticulospinal activation to trapezius muscle activity during exposure to an acute psychosocial stressor. Twenty-five healthy adults were exposed to startling acoustic stimuli (SAS) while performing a motor task during periods of low and high psychosocial stress. Acoustic startle reflexes (ASRs) were recorded in the upper trapezius during low intensity contractions using both surface and intramuscular electromyography. Exposure to the stressor increased subjective and physiological measures of arousal (P < 0.01). The majority of participants demonstrated inhibitory ASRs, whereas a small subgroup with significantly higher trait anxiety (n = 5) demonstrated excitatory ASRs in the low stress condition. Changes in synaptic input for inhibitory ASRs were confirmed by decreases in the discharge rate of single motor units in response to the SAS. ASRs decreased in magnitude for all participants during exposure to the acute psychosocial stressor. These findings suggest that the reticular formation has predominately inhibitory effects on the human upper trapezius during an ongoing motor task and that disinhibition caused by psychosocial stress may contribute to augmentation of trapezius muscle activity. Further research is required to investigate mechanisms underlying the complex ASRs characterized by this study, particularly the phase reversal to excitatory responses observed among more anxious individuals.

New & noteworthy: This study is the first to quantify stress-evoked changes in the acoustic startle reflex in the upper trapezius muscle of humans, and our findings reveal a complex pattern of inhibitory and facilitatory responses consistent with observations in nonhuman primates. We further demonstrate that psychosocial stress consistently reduces the amplitude of these responses. These findings have implications for the control of motor behaviors in response to stress.

Keywords: electromyography; motor units; startle reflex.

Fig. 1.

Sequence of experimental tasks and stimuli is illustrated for an individual trial (A) and the experimental protocol (B). The experimental protocol was explained during an initial familiarization. Following equipment set-up, habituation comprised 6 startling acoustic stimuli (SAS) with no other task requirements. Task practice comprised 8–10 individual trials to practice the force target matching and pinch reaction time (RT) tasks with no SAS. Low stress and high stress conditions each included 4 blocks of 10 individual trials, with the SAS replacing the 50-ms pinch task auditory cue in 30% of trials. Vertical arrows indicate collection time points for arousal measures (note that time is not shown to scale). STAI-S, Spielberger State-Trait Anxiety Index, State Score; MAP, mean arterial pressure; HR, heart rate; B, baseline; L, low stress; H, high stress.

Fig. 2.

Representative data illustrating the cumulative sum (CUSUM) processing technique. An individual response to a SAS in the left upper trapezius is shown before (A) and after (B) rectification. All rectified SAS responses in a given condition (gray lines) were averaged (black line, C). The averaged response after CUSUM processing is shown in D. A response was identified when the vertical distance between 2 turning points (sign change in slope) was greater than those identified in the prestimulus period. The response onset (On) was defined as the first turning point. The response amplitude (Amp) was defined as the vertical distance between 2 consecutive turning points. The response duration (Dur) was defined as the horizontal distance between 2 consecutive turning points. The strength (Str) of a response was calculated as its amplitude divided by its duration multiplied by 100, representing the percentage of maximum excitation or inhibition. This technique allows for identification of multiple excitatory or inhibitory responses. In this example, the first response (On1, Amp1, Dur1, and Str1) is inhibitory, and the second response (On2, Amp2, Dur2, and Str2) is excitatory. Vertical dashed lines represent the onset of the startling acoustic atimulus (SAS).

Fig. 3.

Changes in perceived anxiety [Spielberger State-Trait Anxiety Index State Score (STAI-S); A] and indexes of physiological arousal, including mean arterial pressure (MAP; B) and heart rate (HR; C) during the experimental protocol. All time points (see Fig. 1) collected for each measure are shown. Time points within each condition were averaged before statistical analyses that compared mean scores for the baseline (B1 and B2), low stress (L1, L2, L3, and L4), and high stress (H1, H2, H3, and H4) conditions.

Fig. 4.

Averaged surface EMG responses and corresponding cumulative sum (CUSUM) plots for representative participants illustrating the 4 major response patterns of the upper trapezius muscle to startling acoustic stimuli (SAS): a single period of inhibition (A), inhibition followed by excitation (B), 2 periods of inhibition (C), and a single period of excitation (D). Participants were categorized based on the direction of the initial phase of the acoustic startle reflex (ASR) observed during the low stress condition. Vertical dashed lines represent onset of the SAS.

Fig. 5.

Strength of the initial phase of the acoustic startle reflex (ASR) during low stress and high stress conditions. ASR response strength was calculated using amplitude and duration estimates from the cumulative sum (CUSUM) analysis. The strength of the initial phase of inhibitory responses significantly decreased from low to high stress, with a similar trend for reduced strength of the initial phase of excitatory responses.

Fig. 6.

Representative data for an inhibitory surface EMG response (A) and corresponding single motor unit (SMU) activity (B) in response to the startling acoustic stimulus (SAS). Vertical dashed lines represent onset of the SAS. SMU analyses were performed only for inhibitory ASRs due to the low number of identifiable SMUs in the excitatory ASR group. Discharge rates (DR) were normalized to the average DR from a 150-ms prestimulus period, and the average response onset for each participant was set as time 0 to account for variability in response latencies. DRs from all SMUs were then averaged in 10-ms bins within each stress condition. Periods of decreased DR were noted in both the low (C) and high (D) stress conditions.