Startle response of human neck muscles sculpted by readiness to perform ballistic head movements

Abstract

1. An acoustic startle stimulus delivered in place of a 'go' signal in a voluntary reaction time (RT) task has been shown previously to advance the onset latency of a prepared distal limb movement without affecting the amplitude of the muscle response or movement kinematics. The primary goal of this study was to use muscles with a larger startle response to investigate whether the startling stimulus only triggered the RT movement or whether some form of interaction occurred between a startle response and a temporally advanced RT movement. 2. Twenty healthy male or female subjects were instructed to react as quickly as possible to an acoustic 'go' stimulus by performing a ballistic head flexion or right axial rotation. The 'go' stimulus was periodically replaced by an acoustic stimulus capable of eliciting a startle reflex. Separate startle-inducing stimuli under relaxed conditions before and after the movement trials served as control trials (CT trials). Bilateral surface electromyography of the orbicularis oculi, masseter, sternocleidomastoid and cervical paraspinal muscles, and head-mounted transducers were used to measure the muscle response and movement kinematics. 3. Muscle activation times in startled movement trials (ST trials) were about half those observed in RT trials, and were not significantly different from those observed in the startle CT trials. The duration of head acceleration was longer in ST trials than in RT trials and the amplitude of both the neck muscle electromyogram (EMG) and head kinematics was larger during ST trials than during RT trials. The EMG amplitude of ST trials was biased upward rather than scaled upward compared with the EMG amplitude of RT trials. 4. Over the 14 ST trials used in this experiment, no habituation of the reflex response was observed in the muscles studied. This absence of habituation was attributed to a combination of motor readiness and sensory facilitation. 5. The results of this experiment indicated that the neck muscle response evoked by a startling acoustic stimulus in the presence of motor readiness could be described as a facilitated startle reflex superimposed on a temporally advanced, pre-programmed, voluntary RT movement. Parallel reticular pathways to the neck muscle motoneurones are proposed as a possible explanation for the apparent summation of the startle and voluntary movement responses.

Figure 1. EMG recordings from the control, startle and reaction time trials of a single subject

A, EMG recordings from the first control (CT) trial. B, EMG recordings from the second CT trial, administered between the flexion and rotation blocks. C, EMG recordings from a startle (ST) trial in which the subject was ready to perform a ballistic flexion movement. D, EMG recordings from a ST trial in which the subject was ready to perform a ballistic axial rotation movement. E, EMG recordings from a RT trial for a flexion movement. F, EMG recordings from a RT trial for an axial rotation movement. The vertical bar between the Accel and ω traces is equivalent to 1 g and 5 rad s⁻¹. OO, orbicularis oculi; MAS, masseter; SCM, sternocleidomastoid; PARA, cervical paraspinal muscles; l, left; r, right; Accel, linear head acceleration at the forehead; ω, angular velocity of the head. The vertical line through all traces of a single trial indicates the onset of either the ‘go’ or the startling tone.

Figure 2. Muscle activation times, ratios and differences for the neck muscles of all subjects

A, mean onset times ± 1 s.d. for the left and right sternocleidomastoid (SCM) muscles during control (CT), flexion (ST and RT) and rotation (ST and RT) trials. Note that onset times during CT and startle (ST) trials were significantly faster than onset times for RT trials. B, similar to previous panel, except data are for the cervical paraspinal (PARA) muscles. C, mean ratio ± 1 s.d. of the ST onset time to the RT onset time (ST/RT) for each muscle as a function of muscle side (left, right) and movement type (flexion, rotation). D, mean arithmetic difference ± 1 s.d. of the ST and RT onset times (RT-ST) for each muscle as a function of muscle side and movement type. E, mean ratio ± 1 s.d. of the left to right onset latency (L/R) for each functional muscle pair as a function of stimulus (ST, RT) and movement type. F, mean arithmetic difference ± 1 s.d. of the left and right onset times (L-R) for each functional muscle pair as a function of stimulus and movement type. Note that the asynchronous onset of the left and right neck muscles during rotation movements, which manifested as a left/right (L/R) ratio greater than 1, was present in both the ST and RT trials.

Figure 3. EMG amplitudes, ratios and differences for the neck muscles of all subjects

A, mean normalized root mean squared (RMS) EMG amplitude ± 1 s.d. of the left and right sternocleidomastoid (SCM) muscles as a function of stimulus (ST, RT) and movement type (flexion, rotation). B, similar to previous panel, except data are for the cervical paraspinal (PARA) muscles. Note the bilateral symmetry during flexion movements and bilateral asymmetry during rotation movements. C, mean ratio ± 1 s.d. of the ST amplitude to the RT amplitude (ST/RT) for each muscle as a function of muscle side (left, right) and movement type. D, mean arithmetic difference ± 1 s.d. of the ST and RT amplitudes (ST-RT) for each muscle as a function of muscle side and movement type. Note the consistent upward bias present in the startle (ST) trials. E, mean ratio ± 1 s.d. of the left to right amplitudes (L/R) for each functional muscle pair as a function of stimulus and movement type. F, mean arithmetic difference ± 1 s.d. of the left and right amplitudes (L-R) for each functional muscle pair as a function of stimulus and movement type. The consistent, within-muscle, L-R difference in rotation trials indicated that the movement was preserved on top of the upward bias introduced by the startle tone.

Figure 4. Absence of habituation to startle during sequential trials

A, mean EMG amplitude ± 1 s.d. of all muscles over the seven sequential startle (ST) trials during the flexion block. The EMG amplitude of each individual subject's muscles was first expressed as a percentage of the amplitude observed in that muscle during the first trial and then the mean was calculated. Note the absence of habituation between the first ST trial (the first trial of a block) and the seventh ST trial (the 20th trial within a block). B, similar to previous panel, but for rotation movements. C, mean amplitude ± 1 s.d. of similarly normalized angular head kinematics. OO, orbicularis oculi; MAS, masseter; SCM, sternocleidomastoid; PARA, cervical paraspinal muscles; l, left; r, right; α, angular acceleration; ω, angular velocity; θ, head angle.