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J Appl Physiol 102: 1574-1586, 2007. First published December 14, 2006; doi:10.1152/japplphysiol.00703.2006
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Interaction between acoustic startle and habituated neck postural responses in seated subjects

Jean-Sébastien Blouin,1 Gunter P. Siegmund,1,2 and J. Timothy Inglis1

1School of Human Kinetics, University of British Columbia, Vancouver, and 2MEA Forensic Engineers & Scientists, Richmond, British Columbia, Canada

Submitted 22 June 2006 ; accepted in final form 7 December 2006


   ABSTRACT
TOP
 ABSTRACT
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 GRANTS
 ACKNOWLEDGMENTS
 REFERENCES
 
Postural and startle responses rapidly habituate with repeated exposures to the same stimulus, and the first exposure to a seated forward acceleration elicits a startle response in the neck muscles. Our goal was to examine how the acoustic startle response is integrated with the habituated neck postural response elicited by forward accelerations of seated subjects. In experiment 1, 14 subjects underwent 11 sequential forward accelerations followed by 5 additional sled accelerations combined with a startling tone (124-dB sound pressure level) initiated 18 ms after sled acceleration onset. During the acceleration-only trials, changes consistent with habituation occurred in the root-mean-square amplitude of the neck muscles and in the peak amplitude of five head and torso kinematic variables. The subsequent addition of the startling tone restored the amplitude of the neck muscles and four of the five kinematic variables but shortened onset of muscle activity by 9–12 ms. These shortened onset times were further explored in experiment 2, wherein 16 subjects underwent 11 acceleration-only trials followed by 15 combined acceleration-tone trials with interstimulus delays of 0, 13, 18, 23, and 28 ms. Onset times shortened further for the 0- and 13-ms delays but did not lengthen for the 23- and 28-ms delays. These temporal and spatial changes in EMG can be explained by a summation of the excitatory drive converging at or before the neck muscle motoneurons. The present observations suggest that habituation to repeated sled accelerations involves extinguishing the startle response and tuning the postural response to the whole body disturbance.

posture; neck muscle reflexes; habituation

POSTURAL RESPONSES RAPIDLY adapt with repeated exposures to the same perturbation in standing (2, 19, 24), seated (3, 34), and supine (2) individuals. This process of adaptation, called habituation (18), typically consists of attenuated muscle activity and related kinematic changes. Startle responses also habituate rapidly to repeated startling stimuli (2, 8, 16, 17, 21, 38, 44), and the time course of this habituation is similar to that observed after repeated whole body accelerations. On the basis of this similarity, it was first proposed (1, 2, 29) and more recently shown (5) that the initially elevated, prehabituation muscle response during the first whole body acceleration is in part a startle response.

Startle responses can be evoked by sudden tactile, vestibular, or auditory stimuli (45) but are most often studied using acoustic stimuli. Axial and appendicular muscles respond to acoustic startle (16), but the strongest and most consistent response occurs in the neck muscles, particularly the sternocleidomastoid (SCM) muscle (8). Since consistent neck muscle responses are also evoked by forward accelerations in seated subjects (3, 4, 6, 32, 34), the neck muscles are well suited for study of the potential interaction between the acoustic startle response and the postural responses elicited by whole body accelerations.

Reflex activation of the neck muscles can be evoked via one or more of the visual, auditory, vestibular, proprioceptive, and cutaneous sensory systems. In some real-world conditions, such as rear-end automobile collisions, all these sensory systems are stimulated, and some form of cross-modal summation likely occurs (45). In the rat, summation of tactile (trigeminal) and acoustic startle responses has been observed at the functional (22) and cellular (27) levels. This summation is thought to occur in the giant neurons of the caudal pontine reticular formation or in the neck muscle motor nuclei in the spinal cord (45). In humans, enhanced eye blinks have been observed with combined tactile and acoustic stimulation (26). In addition, summation of muscle activity from voluntary reaction-time tasks and acoustic startle has been observed in the SCM muscle (30). This combination of animal and human findings suggests that summation of postural and acoustic stimuli can occur, but appropriate testing of this hypothesis remains to be done.

We conducted two experiments to determine how the acoustic startle response interacts with the habituated neck postural response elicited by forward accelerations of the whole body. In experiment 1, seated subjects were first habituated to the forward acceleration and then exposed to the acoustic and acceleration stimuli simultaneously. We hypothesized that the superposition of a loud sound over a forward acceleration would restore the neck muscle activity and kinematic responses to their prehabituated levels. In experiment 2, the delay between the forward acceleration and the loud sound was varied to examine how the two stimuli combine to generate the neck postural response. We hypothesized that shorter interstimulus delays (earlier tones) would shorten muscle onset latencies, because onset would be controlled by the auditory startle response. Longer interstimulus intervals, on the other hand, would show muscle onset latencies similar to those observed when the sled acceleration was presented in isolation, because under these conditions, onset would be controlled by the whole body sled acceleration stimulus.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 GRANTS
 ACKNOWLEDGMENTS
 REFERENCES
 
Subjects

The experiment involved 30 subjects (Table 1) who had no history of whiplash injury, medical conditions that impaired sensory or motor function, or prolonged neck or back pain during the preceding 2 yr. Subjects were asked to complete the neck disability index questionnaire (39), a 10-item questionnaire to record disability levels due to neck pain in daily activities. They did not ingest caffeine or nicotine for 2 h before the experiment. All subjects gave their written informed consent before the present study. The procedures were approved by the University of British Columbia Clinical Research Ethics Board and conformed to the Declaration of Helsinki.


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  		Table 1. Subject age and physical characteristics

 
Instrumentation

Electromyographic (EMG) activity in the SCM, scalenus (Scal), and cervical paraspinal (Para) muscles was recorded bilaterally using disposable 10-mm pregelled (Ag-AgCl) surface electrodes (Bortec, Calgary, AB, Canada) and an amplifier (x500 preamplifier gain; Myosystem 1400, Noraxon, Scottsdale, AZ). All surface electrodes were positioned on the muscle belly and oriented parallel to the muscle fibers. The SCM electrodes were placed obliquely half the distance between the mastoid process and the sternal notch. The Scal surface electrodes were placed on a slightly oblique angle just above the midclavicle, posterior to the cleidal part of the SCM and anterior to the upper trapezius muscle. The PARA electrodes were placed parallel to the spine, 2 cm laterally from midline at the level of C4.

Head acceleration was measured with a nine-accelerometer array (±20 g; model 8302B20S1, Kistler, Amherst, NY) arranged in a 3-2-2-2 configuration (25). The array was secured to the subject's head with a custom-made head gear (Fig. 1). The mass of the head instrumentation package was 324 g, including straps and 40 cm of cable. Torso acceleration was measured using a triaxial accelerometer (±7.5 g; model 34103A, Summit, Akron, OH) and a triaxial angular rate sensor (±100 rad/s; DynaCube, ATA Sensors, Albuquerque, NM). Both torso transducers were mounted onto an aluminum plate, which was fastened midsagittally to the chest immediately below the manubrium with adhesive and straps over the shoulders. The mass of the torso instrumentation was 216 g. Sled acceleration was measured with a uniaxial accelerometer (±100 g; model JTF3629-05, Sensotec, Columbus, OH) oriented horizontally along the axis of motion. Displacements were measured with a motion analysis system (Northern digital 3020, Optotrak, Waterloo, ON, Canada) and nine markers placed on the head gear, torso transducers, and sled. The root-mean-square (RMS) accuracy of the position measurements from the Optotrak system was <0.1 mm, and, on the basis of marker separation, the RMS accuracy of the calculated angles was <0.1°. EMG signals were band-pass filtered at 15–500 Hz and transducer signals were low-pass filtered at 500 Hz before being simultaneously sampled at 2 kHz. Optotrak markers were acquired at 100 Hz per marker.


Figure 1
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  		Fig. 1. Test configuration showing sled and car seat as well as locations of head and torso accelerometers, Optotrak markers, horn, and laboratory reference frame (x, z). Inset: close-up oblique view of configuration of 9-accelerometer array on the head gear. Neck EMG electrodes are not shown.

 
Test Procedures

Before testing, the locations of the head and torso accelerometers and Optotrak markers were digitized relative to various anatomic landmarks (glabella, upper incisors, vertex, opisthocranion, occiput, external acoustic meati, and bilateral lower rims of the orbits) with a three-dimensional digitizer (model B08-02, FaroArm, Lake Mary, FL; ±0.30-mm single-point accuracy). This process established the position and orientation of the head transducers relative to the Frankfort plane and allowed resolution of the kinematics to an anatomically relevant location.

Subjects were seated in a 1991 Honda Accord car seat with the head restraint removed to avoid head contact during the perturbation. The seat was mounted on a custom-fabricated sled powered by two feedback-controlled linear induction motors (model IC55-100A7, Kollmorgen, Kommack, NY). The sled generated no audible or mechanical preperturbation signals that could be used by the subjects to predict the onset of the perturbation. No practice or demonstration trial of the sled movement was presented to the subjects before the experiment. Subjects were told they would be exposed to whole body accelerations and loud acoustic tones. They were not told how many trials or when the combined startle-whole body acceleration would be presented. Subjects were seated on the sled for ~15 min before testing to allow them sufficient time to adopt a comfortable posture. Immediately before testing, subjects were instructed to sit normally, face forward, rest their forearms on their lap, and relax their face and neck muscles.

Experiment 1.   Fourteen subjects (Table 1) were exposed to 16 sequential forward horizontal sled accelerations [peak linear acceleration (apeak) = 1.55 g (SD 0.03), pulse duration ({Delta}t) = 59.0 ms (SD 0.3) ms, change in velocity ({Delta}v) = 0.499 m/s (SD 0.003)] spaced randomly 25–45 s apart. After the acceleration pulse, the sled remained at its peak speed (0.5 m/s) for 500 ms before decelerating at ~0.1 g to rest. With no practice or demonstration trials, subjects first underwent 11 sequential sled-only perturbations (P1–P11) to achieve a stable habituated response (3, 34). During the remaining five sled accelerations (PS1–PS5), a loud auditory tone [1 kHz, 124-dB sound pressure level (SPL), 40-ms duration] was superimposed on the sled acceleration. Neck muscle onset latencies have been shown to be 18 ms shorter, on average, to this acoustic stimulus than to whole body acceleration (28); thus the onset of the tone occurred 18 ms after the onset of sled acceleration. At 25–45 s after PS5, the subjects received a single loud acoustic tone (S1) without the sled perturbation.

Experiment 2.   Sixteen subjects (Table 1) were exposed to 29 forward horizontal sled perturbations of the same magnitude and spacing used in experiment 1. As described for experiment 1, subjects first underwent 11 sled perturbations to achieve a stable habituated response. Of the remaining 18 trials, 15 consisted of combined sled acceleration-tone trials (1 kHz, 124-dB SPL, 40-ms duration), with the onset of the tone at 0, 13, 18, 23, or 28 ms after the onset of sled acceleration. Three repetitions of each delay were randomly presented, with 3 sled-only trials randomly inserted among the 15 combined sled-tone trials. As in experiment 1, subjects also received a tone-only stimulus (S1) after trial 16.

Reference Frames

All kinematic data were resolved to the laboratory reference frame. The z-axis of the global reference frame was defined parallel to the direction of Earth's gravity and positive downward. The x-axis was defined parallel to the longitudinal axis of the sled acceleration and positive forward. The y-axis was positive to the right. Flexion and extension of the head-neck and torso in the sagittal plane occurred about the y-axis, with extension being positive and flexion negative.

Head kinematics were resolved to an origin at the head's center of mass (CoM), which was estimated to lie in the midsagittal plane, rostral to the interaural axis by 17% of the distance between the interaural axis and the vertex (23). Torso kinematics were resolved to a point in the midsagittal plane at the superficial junction of the sternum and manubrium.

Data Reduction

The onset of a muscle's activity was determined using a log-likelihood-ratio algorithm (35, 36). Onset times were then confirmed visually and adjusted manually in <5% of trials. The RMS of each muscle's EMG signal was calculated using a 20-ms sliding window, and the peak RMS EMG and time at peak were determined. The preperturbation RMS EMG calculated for the 100 ms preceding the forward acceleration was removed from the peak EMG activity. For experiment 1, peak RMS values were normalized to (i.e., divided by) trial 1 (P1). The EMG responses were normalized to trial 1 to determine whether the combined sled-tone stimuli would restore the EMG responses to trial 1 levels. For experiment 2, the peak RMS values were normalized to the averaged peak RMS amplitude from trials 9–11 (the last 3 habituation trials) for the corresponding muscle. This normalization procedure was chosen to compare the amplitude of the EMG responses triggered by the sled-tone stimuli presented at various delays with the amplitude of the habituated EMG responses.

Because the head and torso accelerometers were sensitive to 0 Hz, the 1-g field from Earth's gravity was subtracted from the data to yield the transient linear accelerations due to the perturbation. To determine the component of the 1-g field on each accelerometer channel, the orientation of each accelerometer over the duration of the perturbation was computed from the Optotrak data. The bias of each accelerometer was then computed from the 100-ms interval preceding the perturbation and was removed from the 1-g field-corrected accelerometer data.

A rigid body transformation was used to resolve head accelerations to the CoM of the head and atlantooccipital joint (AOJ; Eq. 1). The AOJ was assumed to be 24 mm posterior and 37 mm inferior to the head's CoM (relative to a local reference frame in which the local x-axis was contained in the Frankfort plane) (31)

Formula 1(1)
where aB is acceleration at point B, aA is acceleration at point A, {alpha} is angular acceleration, {omega} is angular velocity, and rB-A is position vector between points A and B.

The head angular acceleration ({alpha}) required for Eq. 1 was computed using the nine corrected accelerometer signals (Eq. 2) (25). The instantaneous angular acceleration thus obtained was independent of the instantaneous angular velocity. Angular acceleration of the head about the y-axis was compared with the sagittal head angular position data computed from the Optotrak for agreement

Formula 1

Formula 2(2)

Formula 2
where {alpha}i is angular acceleration along axis i, ai is acceleration at accelerometer i, and {rho}i is distance between accelerometers.

A subject's initial head and trunk position and orientation were determined from the Optotrak markers over a 100-ms period preceding the perturbation. A subject's dynamic response was then characterized by peak values of various kinematic variables. Peak angular displacements of the head and torso were determined from the Optotrak markers located on the head and torso gear. Retraction was defined as the maximum horizontal rearward translation of the AOJ relative to the manubrium (33). Head angular velocity was computed using the first time derivative of head angular position. Finally, the onset of horizontal head and torso movements was determined directly from the transformed accelerometer data using a finite-differences algorithm (28).

Statistical Analysis

Experiment 1.   One-way repeated-measures analyses of variance (ANOVAs) were used to examine changes in the timing of the muscle response (onset and peak) and in the amplitude of the peak kinematic variables. Three levels were used for each ANOVA: the first trial response (P1), the habituated response (average of P7–P11), and the first combined sled-tone response (PS1). For the muscle amplitude analyses, normalization to trial 1 response eliminated the variance in the trial 1 response (all P1 responses = 1); therefore, one-sample t-tests were used to assess whether the normalized habituated response (average of P7–P11) was significantly different from trial 1, i.e., significantly different from 1. Differences between the normalized habituated responses (P7–P11) and the normalized perturbation-tone responses (PS1) were then assessed using paired t-tests. Subsequent changes to all of the muscle and kinematic variables during the five combined-stimulus trials (PS1–PS5) were assessed using one-way repeated-measures ANOVAs with five levels.

Experiment 2.   Changes in the muscle timing and kinematic amplitudes for the five different sled-tone delays (averaged for the 3 similar trials) were compared using one-way repeated-measures ANOVAs. In addition to the five delay conditions (D0, D13, D18, D23, and D28), two sled-only conditions were also included in the analyses. The first sled-only condition (PA) was the average of trials 9–11 (the last 3 trials of the habituation), and the second sled-only condition (PB) was the average of the three no-tone trials interspersed among the delay trials. For the muscle amplitude analyses, all conditions were first normalized by the PA condition, and then differences between muscle amplitude for the PA and PB conditions were examined using one-sample t-tests. Because the muscle amplitude data for the five delay conditions were not normally distributed (P < 0.05, Shapiro-Wilks test), one-way rank-based repeated-measures ANOVAs were used to analyze differences in peak muscle amplitude between PB and the five delay conditions (46).

Since no changes in amplitude between the left- and right-side muscle data were found, data from the left and right muscles wereaveraged before statistical testing. All statistical tests were performed using Statistica (version 6.1, Statsoft, Tulsa, OK), and post hoc comparisons for the ANOVAs were performed using Tukey's test. Statistical significance was set at P = 0.05.


   RESULTS
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 GRANTS
 ACKNOWLEDGMENTS
 REFERENCES
 
Experiment 1: Sled Acceleration Habituation and Superposition of Startling Tone

Subjects adopted a similar initial posture for the P1, P7–P11, and PS1–PS5 trials. Initial horizontal head-trunk position (–81.1 ± 20.5 mm) and initial head angle (10.5 ± 4.6°) remained unchanged across all conditions, although initial trunk angle was more extended for the P7–P11 (32.7 ± 6.7°) and PS1 (32.6 ± 6.7°) trials than for the P1 trial (30.5 ± 6.4°, P < 0.01). No subsequent changes in initial trunk angle were observed across the repeated whole body acceleration-tone trials (32.6 ± 6.7°).

The whole body sled acceleration induced a stereotypical response in all subjects (Fig. 2). No muscle activity in anticipation of the sled acceleration or combined sled-tone stimulus was observed in any subjects. The onsets of head and torso horizontal acceleration were not affected by habituation or by the subsequent superposition of a startling tone. On average, the onset of sled acceleration preceded the onset of horizontal torso acceleration by 24 ± 5 ms and the onset of horizontal head acceleration by 35 ± 10 ms.


Figure 2
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  		Fig. 2. Sample EMG and kinematic data from a single subject for trial 1 (P1), trial 9 (middle trial of P7–P11), and trial 12 (PS1). {circ}, Kinematic peaks used in the analysis. Vertical scale bars are aligned with onset of perturbation and represent 15 m/s2, 40 mm, 200 rad/s2, 2 rad/s, and 15°. SCM, sternocleidomastoid muscle; Scal, scalenus muscle; Para, cervical paraspinal muscle; l, left; r, right; a, linear acceleration; {alpha}, angular acceleration; {omega}, angular velocity; {theta}, angular position; x, horizontal direction; z, vertical direction; AOJ, atlanto-occipital joint; CoM, center of mass.

 
All three neck muscles exhibited habituation to the sled acceleration, and 5 of the 9 head and neck kinematic parameters changed significantly over the first 11 trials (Tables 2 and 3). Peak muscle activity decreased 28–45% from P1 to P7–P11, but neck muscle onset times remained unchanged (Table 2, Fig. 3). Compared with P1, the altered kinematic responses in P7–P11 consisted of decreases in horizontal AOJ acceleration (–21%) and trunk extension angle (–14%) and increases in trunk acceleration (+10%), head angular velocity (+12%), and head extension angle (+22%; Table 3, Fig. 4).


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  		Table 2. EMG onset times, peak RMS times, and normalized peak RMS amplitudes

 

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  		Table 3. Peak amplitude of selected kinematic variables

 

Figure 3
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  		Fig. 3. Trial-by-trial mean (SD) of neck muscle responses [peak root mean square (RMS) amplitude and onset latency] during habituation to repetition of a forward perturbation (P1–P11, bullet) and reversal of habituation with superposition of a loud noise (PS1–P5, {circ}). For display purposes, peak RMS amplitude of neck muscle responses was normalized with respect to responses observed for trial 1.

 

Figure 4
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  		Fig. 4. Trial-by-trial mean (SD) of selected kinematic responses during habituation to repetition of a forward perturbation (P1–P11, bullet) and reversal of habituation with superposition of a loud noise (PS1–P5, {circ}). For display purposes, all kinematic variables were normalized with respect to responses observed for trial 1. x, Horizontal direction.

 
Superposition of the startling tone and sled acceleration in PS1 reversed the habituation of all three neck muscles. Peak muscle activity in PS1 was significantly greater than in the habituated levels (by 53, 61, and 51% for SCM, Scal, and Para, respectively) and was not significantly different from the peak activity observed in P1 (Table 2). Compared with the first sled-only acceleration, onset latencies during PS1 were 9–12 ms shorter and peak activity occurred 21–29 ms earlier in all three muscles.

Of the five kinematic parameters affected by habituation, four parameters (AOJ acceleration, head angular velocity, head angle, and trunk angle) returned to levels during PS1 that were not significantly different from those during P1 (Table 3, Fig. 4). Paradoxically, the habituation-related changes in peak trunk acceleration increased with the addition of the startling tone. Of the kinematic parameters not previously affected by habituation, only the first peak in the head angular acceleration ({alpha}1) was significantly larger in PS1 than in P1.

The increased neck muscle activity observed with the addition of the startling tone did not change with repeated exposures to the combined sled-tone stimuli (PS1–PS5; Table 2, Fig. 3). The kinematic responses, with the exception of peak trunk angle, were also not affected by repeated sled-tone exposures (Table 3, Fig. 4).

Experiment 2: Variable Sled Acceleration-Tone Delays

Subjects again adopted consistent initial head and trunk positions before the five delay conditions (D0, D13, D18, D23, and D28) and the two sled acceleration-only conditions (PA and PB). The initial horizontal head-trunk position (–81.1 ± 15.6 mm) and initial head angle (11.8 ± 6.7°) were similar to those observed in experiment 1. Initial trunk angle, however, was, on average, 0.7° more extended for the PA condition than for all other conditions (33.5 ± 6.7° vs. 32.8 ± 6.5°, P < 0.01). The onset of horizontal head acceleration (37 ± 8 ms) and horizontal torso acceleration (24 ± 5 ms) was not affected by the different delay conditions and was similar to that in experiment 1.

The onset of activity in all three muscles occurred earlier during the combined sled-tone stimuli than during the sled acceleration-only conditions (Table 4, Fig. 5). There were no differences in onset latencies between the two sled acceleration-only conditions. Within the five delayed conditions, all neck muscles exhibited a similar pattern of changes in onset times (Fig. 5B). Onset times did not vary between D18, D23, and D28, and the average onset times for these three delays were 3–8 ms shorter than the average for the sled-only conditions. Onset times were an average 3 ms shorter for D13 and an additional 4 ms shorter for D0 than the three long delays (Table 4). This pattern was most pronounced in the SCM muscles and least pronounced in the Scal muscles.


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  		Table 4. EMG onset times, peak RMS times, and normalized peak RMS amplitudes

 

Figure 5
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  		Fig. 5. Changes in neck muscle onset latency for the forward perturbation performed in isolation and in combination with the acoustic stimulus presented at various delays. A: sample EMG data from left (dark traces) and right (gray traces) SCM muscles of 1 subject. Time 0 (dashed line) aligned with onset of SCM muscle activity in the PA condition. Thin black vertical line, onset of perturbation; gray vertical line, onset of acoustic stimulus. B: mean (SD) of neck muscle onset latencies for the forward perturbation performed in isolation (PA and PB, bullet), in combination with the acoustic stimulus presented at various delays (D0–D28, {circ}), and acoustic stimulus only (ST, {square}). Time 0 aligned with muscle onset in the PA condition. Dx, x-ms delay; PA, 1st perturbation-only condition; PB, 2nd perturbation-only condition; ST, startle only.

 
Similar to experiment 1, the peak EMG amplitudes for all neck muscles were larger during most of the combined sled-tone conditions than during the sled acceleration-only trials (Table 4). There were, however, no significant differences in peak EMG amplitudes between the five delay conditions. Peak EMG amplitudes for the SCM and Scal muscles also occurred 11–18 ms earlier during the combined stimuli than during the sled-only conditions, but again there were no differences in peak EMG times between the five delay conditions.

Differences in the kinematics between the combined stimuli and the sled acceleration-only condition were similar to those observed in experiment 1 (Table 5, Fig. 6). AOJ acceleration was again increased (22–32%) and retraction decreased (8 to 11%) by addition of a startling tone to the whole body sled acceleration. In addition, peak head angular position and velocity decreased by 8–15% during the combined stimuli compared with the sled acceleration-only conditions. As with EMG amplitude, there were no differences in the amplitude of any kinematic parameters between the five delay conditions or between the two sled-only conditions.


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  		Table 5. Peak amplitude of selected kinematic variables

 

Figure 6
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  		Fig. 6. Mean (SD) of kinematic responses following forward linear accelerations ({blacktriangleup}) and following superposition of a loud sound over the perturbation with various delays ({circ}). Kinematic variables were normalized with respect to PA (average response observed for P9–P11). No significant differences were observed between the various sled-startle delay conditions.

 
Exposure to the startling tone in isolation (S1) produced muscle response amplitudes that were much smaller after five combined sled-tone trials than after the sled acceleration-only or the sled-tone trials presented before or after S1. In one subject, there was no EMG response to the tone-only trial; in most other subjects, EMG was visible only in some neck muscles (Table 6). On the basis of the subsets of muscles that exhibited responses to the startling tone in isolation, the average onset time of the neck muscles occurred 16–20 ms (average 18 ms) earlier than for the sled acceleration-only trials.


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  		Table 6. EMG onset times for startle-only trial

 

   DISCUSSION
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
GRANTS
 ACKNOWLEDGMENTS
 REFERENCES
 
Repeated exposures to an abrupt forward acceleration produced attenuated neck muscle responses consistent with habituation in anterior and posterior neck muscles. On the basis of the lower peak head accelerations and higher peak head displacements observed after habituation, the habituation process appeared to reduce the stiffness of the connection between the head and trunk. These muscle and kinematic changes are similar to those observed in earlier studies of habituation in seated subjects (3, 34). After this habituation, subjects were exposed to the same sled acceleration plus a loud, startling tone capable of evoking a startle reflex in neck muscles (30). Brief, intense acoustic stimuli (<7-ms duration, >120-dB SPL) can also evoke vestibular myogenic potentials in tonically active neck muscles (12–15, 42, 43). However, vestibular-evoked myogenic potentials are attenuated with tone bursts >10 ms, and tonic activity in the muscle of interest is required to see the auditory saccular reflex (12, 13, 43). Since the tone was 40 ms long and the neck muscles were initially quiet in our experiment, we believe that the saccular reflex played a minor role or no role in the modification of the sled-evoked postural responses. In addition, no sign of EMG activity could be detected on individual or averaged traces around the 13- to 23-ms interval, when the saccular reflex is typically observed. Hence, we believe the parameters of our acoustic stimulus allowed us to evoke a startle-mediated muscle response, while the external forces applied by the sled acceleration remained constant.

The addition of the startling tone restored the EMG amplitudes of all three neck muscles and the peak amplitudes of four (of 5) habituation-affected kinematic parameters to levels not significantly different from those measured before habituation, i.e., during the first sled acceleration-only trial. Except for the peak trunk acceleration that was not restored, these results are consistent with a combined postural-startle response during the first perturbation (1, 2, 5, 29). The main difference between the postural-startle response evoked by the first sled-only perturbation and the postural-startle response evoked by the sled-tone stimuli resides in the sensory afferents mediating the startle response. The startle response to the first sled-only perturbation was presumably triggered by somatosensory or vestibular afferents. During repeated exposures to the sled acceleration, the somatosensory/vestibular startle component of the response habituates. Our results demonstrate that a startle response triggered by a loud acoustic stimulus can interact with the neck postural responses elicited by the sled acceleration. This acoustically triggered startle response increases neck muscle cocontraction during a whiplash-like perturbation, leading to a stiffer head-neck system, as suggested by the larger forward head acceleration and smaller head retraction during exposure to the combined stimuli. These observations further support the hypothesis that the startle reflex triggers a head-neck defensive response to a sudden perturbation (45).

Summation of the Startle and Sled Perturbation Stimuli

The simplest interaction between the postural and startle response evoked by the sled perturbation and acoustic stimuli, respectively, is a summation. Summation of cutaneous and acoustic stimuli has been observed previously in startle responses in the rat at the functional and cellular levels (22, 27). These studies, however, focused on summation of the response amplitude, rather than shifts in muscle onset times. The superposition of the startling acoustic stimulus over the sled acceleration increased neck muscle responses to levels similar to those elicited by the first sled-only perturbation. In addition, the onset times of all neck muscles were 7–12 ms shorter during the sled-tone trials than during the first and habituated sled acceleration-only trials. This suggests that the previously reported 18-ms delay was inaccurate or the afferent volleys evoked by the combined sled-tone stimulus accelerated the combined postural-startle response. Since a similar difference (18 ms average) in onset latencies between the sled acceleration-only and tone-only trials was observed in the present experiment (Table 6), the combination of the stimuli appears to be responsible for the advanced muscle onset time. Advanced onset times have been observed in acoustically startled volunteers performing simple reaction-time tasks (9, 10, 30, 37) and are reportedly shifts from voluntary latencies to startle reflex latencies. Similarly, the advanced muscle responses to the combined stimuli could suggest that the startle initiates a faster execution of the neural responses triggered by a sudden whole body forward acceleration. Although attractive and simple, this hypothesis does not explain the results observed in experiment 2.

Experiment 2 examined the effect of five delays ranging from 0 to 28 ms between the onset of the sled acceleration and the onset of the startling tone. For tone delays less than the 18-ms delay used in experiment 1, there was a further shortening of muscle onset times: onset occurred 3 ms earlier when the delay decreased 5 ms from D18 to D13 and an additional 4 ms earlier when the delay decreased another 13 ms from D13 to D0. The absence of a significant difference between the onset times for D0 and the tone-only condition suggests that muscle onset during D0 was driven primarily by the acoustic stimulus. The absence of a neck muscle response time locked to the acoustic startle stimulus indicates that the acoustic startle stimuli did not trigger the earlier execution of the muscle responses to the sled-startle stimuli. For ≥18-ms interstimulus delays, there appeared to be a ceiling effect, even though these onset latencies were still 3–8 ms shorter than for the sled acceleration-only trials (PA and PB). This suggests that the afferent volley from the acoustic stimulus, although it was timed to arrive at the sensorimotor interface after the afferent volley from the sled acceleration for >18-ms delays, still interacted with the postural response in some manner that accelerated muscle onset.

Brown et al. (7) observed shifts in lower limb muscle onset latencies of 40–60 ms to a startling auditory stimulus when these muscles were posturally active. They argued that the startle response consisted of various waves of activity, each of which could not always be observed. If this argument holds true, then a subthreshold afferent wave from our sled acceleration or startling tone reaches the reticular neurons or the neck muscle motoneurons earlier than previously thought and perhaps facilitates the subsequent sled acceleration or acoustically triggered volley. Summation of subthreshold afferent volleys from each of the combined sled-tone stimuli could generate an excitatory postsynaptic potential that is large enough to trigger an action potential (20) and yield earlier activation of the neck motoneurons. Although the present experiment cannot determine where the interaction between the two stimuli occurred, we believe that it provides compelling evidence that the startle- and sled-evoked postural responses sum to create the neck muscle responses during an unexpected postural disturbance.

Absence of Habituation to the Combined Stimuli

The absence of habituation to the combined sled-tone stimuli is at odds with the typically rapid habituation associated with sequential presentation of a loud acoustic stimulus (2, 8, 38). A similar lack of habituation to a loud acoustic stimulus has been observed in subjects engaged in a reaction-time paradigm (11, 30), wherein it was proposed that a subject's readiness to perform a reaction-time task facilitated the sensorimotor system and interfered with the inhibitory response that presumably underlies habituation. Although subjects in the present study could not anticipate the exact timing of the upcoming sled acceleration, they knew that it would ultimately occur, and they might have increased their readiness. This increase in readiness may have interfered with the normal habituation process. Alternatively, habituation may be a more global response, and the afferent volley evoked by the normally startling acoustic stimulus encountered an already inhibited sensorimotor system. Such persistent habituation has been observed when the sensory modality changed between acoustic and tactile in the rat (40), although in the present study we added a new modality, rather than changed modalities. Moreover, homosynaptic depression in the giant neurons of the caudal pontine reticular formation has been observed in a rat preparation exposed to sequential stimulation of trigeminal or acoustic afferents (27, 41). If this homosynaptic depression is the cellular mechanism responsible for habituation, then other sensory modalities that converge onto these neurons encounter a prehabituated neuron and no further habituation, even to a new stimulus modality, would be expected.

Regardless of the explanation, the absence of a "second" habituation suggests that the superposition of a loud acoustic stimulus did not reverse habituation but, rather, restored the magnitude of the afferent volley reaching the neck motoneurons without altering the magnitude of the sled acceleration. The addition of a startling acoustic stimulus to a body disturbance in postural studies may allow researchers to better replicate in a laboratory environment the complex events during the first exposure to a novel postural perturbation. Such a protocol would be particularly useful for studying unexpected transient whole body perturbations such as those that occur while an indiviual stands on a bus or is involved in a car collision.

Other Observations

Peak trunk acceleration was the only variable not restored to preperturbation levels with the addition of the loud tone. Peak trunk acceleration occurred before forward head acceleration increased to any significant degree (Fig. 2). Since the onset of muscle activity (78–83 ms during P1 and P7–P11) occurred at about the same time as peak trunk acceleration, the change in peak trunk acceleration between P1 and the habituated trials (P7–P11) was likely not caused by habituation of the muscle response. Instead, it may be related to the 2° increase in initial trunk angle we observed between the first and habituated trials, with no further change during the combined sled-tone trials (PS1–PS5). A larger initial trunk angle is consistent with the subjects relaxing into the seatback after a few trials and improving the coupling between the torso and the seatback. This improved coupling could explain the larger peak trunk accelerations. Thus the only kinematic parameter that did not support our hypothesis appears to have been affected by a change in initial posture, rather than habituation.

The sled acceleration and acoustic stimuli used in the present experiments were not reported as painful by the participants. Since habituation only occurs to nonnoxious stimuli, the present results may not apply to more severe sled accelerations or louder tones, which could generate a sensitization, rather than a habituation. We also limited our study to sled acceleration followed by an acoustic stimulus. It is not known whether other combinations of stimuli, or even the reverse combination, would yield the same results.

In summary, the results of the present experiments show that the startle component of the neck muscle response triggered by a first exposure to a whole body sled acceleration can be restored by the superposition of a startling sound on the sled acceleration in habituated subjects. These observations further suggest that habituation to repeated sled accelerations involves extinguishing the startle response and tuning the postural response. The earlier and larger neck muscle response elicited by the combination of sled acceleration and startle stimuli can be explained by a summation of the separate afferents triggered by each stimulus. The modified neck muscle response evoked by this summation increases the coupling between the head and neck and is consistent with the protective role of the startle response.


   GRANTS
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 GRANTS
ACKNOWLEDGMENTS
 REFERENCES
 
This research was funded by the Natural Sciences and Engineering Research Council of Canada (J. T. Inglis), Canadian Institutes of Health Research (J. S. Blouin), Michael Smith Foundation for Health Research and British Columbia Workers Compensation Board (J. S. Blouin), a British Columbia Neurotrauma Grant (J. T. Inglis, G. P. Siegmund, and J. S. Blouin), and MEA Forensic Engineers & Scientists (G. P. Siegmund).


   ACKNOWLEDGMENTS
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 GRANTS
 ACKNOWLEDGMENTS
REFERENCES
 
We thank Jeff Nickel and Mircea Oala-Florescu (MEA Forensic Engineers and Scientists) for help in building the sled and equipment used for this experiment.


   FOOTNOTES
 

Address for reprint requests and other correspondence: G. P. Siegmund, MEA Forensic Engineers & Scientists, 11-11151 Horseshoe Way, Richmond, BC, Canada V7A 4S5 (e-mail: gunter.siegmund{at}meaforensic.com)

The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.


   REFERENCES
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 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 GRANTS
 ACKNOWLEDGMENTS
 REFERENCES
 

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