J Neurophysiol 89: 1857–1863, 2003.
First published December 18, 2002; 10.1152/jn.00852.2002.
Altered Triggering of a Prepared Movement by a Startling Stimulus
Anthony N. Carlsen, Michael A. Hunt, J. Timothy Inglis, David J. Sanderson, and Romeo Chua
School of Human Kinetics, University of British Columbia, Vancouver, British Columbia V6T 1Z1, Canada
Submitted 25 September 2002; accepted in final form 6 December 2002
Carlsen, Anthony N., Michael A. Hunt, J. Timothy Inglis, David
J. Sanderson, and Romeo Chua. Altered triggering of a prepared
movement by a startling stimulus. J Neurophysiol 89: 1857–1863, 2003.
First published December 18, 2002; 10.1152/jn.00852.2002. An experiment is reported that investigated the effects of an auditory startling
stimulus on a compound movement task. Previous findings have shown
that, in a targeting task, a secondary movement can be initiated based on
the proprioceptive information provided by a primary movement. Studies
involving the presentation of a startling stimulus have shown that in
reaction time (RT) tasks, prepared ballistic movements could be released
early when participants are startled. In the present study we sought to
determine whether the secondary component in an ongoing movement
task, once prepared, could also be triggered by a startling stimulus.
Participants performed a slow active elbow extension (22°/s), opening
their hand when the arm passed 55° of extension from the starting point.
An unexpected 124 dB startle stimulus was presented 5, 25, or 45° into
the movement. Findings showed that, when participants were startled, the
secondary component was triggered despite incongruent kinesthetic information. However, this only occurred when the startle was presented
late in the primary movement. This suggests that the secondary movement was not prepared prior to task initiation, but was “loaded” into
lower brain structures at some point during the movement in preparation
to be triggered by the CNS. This occurred late in the movement sequence,
but ⱖ400 ms prior to reaching the target. These findings indicate that, in
addition to ballistic RT tasks, a startle can be used to probe response
preparation in ongoing compound movement tasks.
INTRODUCTION
The concept of a motor program has been used as a model
to reconcile the suggestion that a ballistic response (see Ghez
1991) can be prepared in advance and “run off” unaffected by
outside influences or peripheral feedback (Keele 1968). A
neural corollary of the motor program has been hypothesized to
be composed of cortical cell assemblies, which are groups of
cortical neurons with strengthened synaptic interconnections
(Wickens et al. 1994). Recent evidence has shown that motor
programs may be triggered by a startling stimulus. The presentation of an unexpected loud acoustic stimulus has been
shown to result in a stereotyped startle response in humans,
including activation of the sternocleidomastoid (SCM) and
orbicularis oculi (OOc) muscles at short latencies (Brown et al.
1991; Davis 1984; Scott et al. 1999; Yeomans and Frankland
1996). However, when it is paired with a reaction time (RT)
task, it has been shown that a startling acoustic stimulus will
also elicit a prepared ballistic response at very short onset
latencies (Valls-Solé et al. 1995, 1999). Two lines of evidence
support the notion of a startle-elicited response. First, the
Address for reprint requests: R. Chua, 210-6081 University Blvd., Vancouver, BC V6T 1Z1, Canada (E-mail: rchua@interchange.ubc.ca).
www.jn.org
response-related electromyographic (EMG) activation pattern
(e.g., Wadman et al. 1979) triggered by the startling stimulus is
similar in both burst duration and timing to that produced when
participants perform the task in the absence of the startling
stimulus (Valls-Solé et al. 1999). Second, task accuracy is
maintained during the startle-elicited response (Carlsen et al.
2000). These observations indicate that the intended prepared
response has been triggered and that it is not simply a later
voluntary response superimposed on an early startle reflex.
Since the response is produced at latencies presumably too
short to involve the motor cortex, it has been suggested that the
response is prepared and stored subcortically and its initiation
is triggered by the startling stimulus (Valls-Solé et al. 1999).
Since the scope of inquiry into the effects of the startle on
prepared movements is limited mainly to RT tasks involving a
prepared ballistic response from a static starting position
(Carlsen et al. 2000; Siegmund et al. 2001; Valls-Solé et al.
1995 1999), it is not known how the presentation of a startling
stimulus might affect an ongoing compound movement task.
Several types of compound movement sequences, such as
typing (Terzuolo and Viviani 1979) and handwriting (e.g.,
Fischman 1984), have been previously examined with results
indicating that the sequences are centrally controlled by a
motor program. However, the use of proprioceptive information in triggering discrete movement sequences has recently
been examined by Cordo (1990) and others (Bevan et al. 1994;
Cordo et al. 1994). Participants performed an active elbow
extension movement (22°/s) and were required to open their
hand within a fixed target area without the use of visual
feedback. Although the time taken to reach the target area
changed in relation to movement distance and resistance imposed, participants were successful in completing the handopening task within the target area. This indicated that some
form of kinesthetic feedback from the elbow extension movement was used to trigger the secondary movement, not simply
time-to-target (Cordo 1990). Later studies showed that information regarding both the elbow joint angle position and
angular velocity were used by the CNS in successfully triggering the secondary movement at the correct position (Bevan et
al. 1994; Cordo et al. 1994 1995).
If the secondary movement (hand opening) in the targeting
task described above is triggered based on kinesthetic information from the primary elbow extension movement (Bevan et
al. 1994; Cordo 1990; Cordo et al. 1994), this suggests that the
secondary movement must have been prepared at some point
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.
0022-3077/03 $5.00 Copyright © 2003 The American Physiological Society
1857
1858
CARLSEN, HUNT, INGLIS, SANDERSON, AND CHUA
prior to its initiation. Preparation could have taken place either
at the same time as the primary movement or at some point
during the execution of the primary task. The purpose of the
present experiment was to determine whether a secondary
movement that is prepared and then initiated on the basis of
proprioceptive information about joint angle from a separate
ongoing movement could be triggered by a startling acoustic
stimulus. If so, the point at which the movement is prepared
and loaded for initiation can be probed based on whether the
secondary response is evoked at a given probe position. We
hypothesized that the secondary movement would be prepared
at some point during the execution of the primary task and that
this point could be probed successfully with the use of a
startling stimulus.
METHODS
Participants
Thirteen right-handed volunteers (5 male, 8 female; ages 26 ⫾ 3 yr)
with no obvious upper body abnormalities or sensory or motor dysfunctions volunteered to participate in the study. All participants gave
informed consent, and the study was conducted in accordance with the
ethical guidelines set by the University of British Columbia.
Participant set-up
Participants sat upright in a comfortable height-adjustable chair
outfitted with an automobile racing harness (Racer Components) to
constrain any movement to the forearm segment. The right arm was
secured, in a semiprone position with the palm facing inward, to a
custom-made aluminum manipulandum that moved in the transverse
plane. The starting position of the arm was 80° of flexion (where 180°
⫽ full extension) at the elbow (indicated by a fixed physical stop) with
the shoulder both flexed and abducted 90°. The medial epicondyle of
the right arm was centered over the axis of rotation of the manipulandum.
Stimuli
The warning tone consisted of three short beeps (100 ms, 1,000 Hz,
82 dB each, separated by 500 ms). Trial stimuli were generated using
a custom-made tone burst generator, which generated a narrow-band
noise pulse (1,000 Hz, 40 ms duration), and presented via a loudspeaker (⬍1 ms rise time) placed directly behind the head of the
participant with intensities of either 84 dB (nonstartle stimulus) or 124
dB (startle stimulus). The stimulus intensities were measured using a
sound-level meter (model CR:252B, Cirrus Research) at a distance of
30 cm from the loudspeaker (approximately the distance to the ears of
the participant).
Training
Participants practiced extending their right elbow at a constant rate
(22°/s) and opening their right hand at a constant target location (55°
of extension from starting point) using a feedback-based training
program presented on a computer monitor placed 1 m in front of the
participant. The position of the manipulandum was represented by a
short (1 cm) vertical line that moved in the horizontal plane, with the
starting position indicated as a position near the left edge of the
screen. The vertical marker line remained fixed at the position at
which hand opening occurred providing target accuracy feedback. A
2° wide target area was represented by a 1-cm-wide blue area in the
same horizontal plane on the monitor. A green arrow placed above the
manipulandum marker moved from slightly left of the starting position, left to right horizontally across the screen at a fixed rate corresponding to an elbow extension velocity of 22°/s. The participants
were instructed to mimic the movement of the green arrow with the
vertical line and to open their right hand when the vertical line passed
through the target area. Once comfortable, participants performed the
movement without the use of this visual feedback and were instead
only given knowledge of results pertaining to opening angle and
movement velocity after each practice trial. Participants were deemed
to be competent at performing the task when they could perform five
consecutive trials without visual feedback in which both elbow velocity and hand opening were within 2° of their respective target
values.
Experimental procedure
Instrumentation
Surface EMG data were collected from the muscle bellies of the
right extensor digitorum longus (EDL), right biceps brachii (BI), right
triceps brachii (TRI), left OOc, and left SCM muscles using bipolar
preamplified Ag/AgCl surface electrodes (Therapeutics Unlimited).
The recording sites were prepared to remove excess debris, thereby
decreasing electrical impedance. The electrodes were oriented parallel
to the muscle fibers and then attached using double-sided adhesive
strips. A grounding electrode was placed on the participant’s left
radial styloid process. EMG data were amplified onsite and the electrodes were connected via shielded cabling to an external amplifier
system (model 544, Therapeutics Unlimited). The signals were fed
from the amplifier and sampled using an analog/digital (AD) interface
(Data Translation DT2821) controlled by a customized program written with LabVIEW software (National Instruments). Data collection
was initiated by the computer program at the start of each trial.
Arm angular displacement data were collected using a potentiometer attached to the pivot point of a custom-made manipulandum.
Hand opening was monitored using a simple finger-tip switch. The
switch consisted of electrically conductive wires powered by a 9-V
battery attached to thin pieces of aluminum, which were then attached
to the thumb and middle finger of the participant’s right hand. The
switch was configured in such a way as to send a signal of 0 V when
it was closed and 9 V when it was open. All signals were digitally
sampled at 2,000 Hz and recorded for later analysis.
J Neurophysiol • VOL
The experimental task was the same as the movement learned
during training: an active elbow extension (22°/s) and an active hand
opening at a target area located 55° into extension. During testing
trials, no on-line feedback was given, although knowledge of results
pertaining to average movement velocity and opening angle were
given following each trial.
Control trials were simply trials in which the participant carried out
the normal protocol of the experiment. A series of warning tones
signified the start of the trial, at which time the participant performed
the task as described above. Participants were advised that fast reaction times were not necessary, but movement soon after the warning
tones was required.
Probe trials consisted of either startle (ST) trials or nonstartle (NST)
trials. ST trials were trials in which the startle stimulus (124 dB) was
given at some point during the trial, whereas NST trials were trials in
which the nonstartle stimulus (82 dB) was given at some point during
the trial. The probe was given in three distinct positions once the
movement was underway, but in only one position on any given trial.
The probe was given either early in the movement (5° of extension
past the starting point), in the middle of the movement (25° of
extension), or late in the movement (45° of extension). Participants
were instructed to ignore any auditory stimulus that occurred.
Participants performed three blocks of 20 trials consisting of 13
control (no probe) trials, 3 ST trials (1 at each of 5°, 25°, and 45° of
extension), and 4 NST trials (2 at each of 25° and 45° of extension).
89 • APRIL 2003 •
www.jn.org
ALTERED TRIGGERING BY STARTLE
1859
The order of the trials was randomized and the participants were not
aware of the testing order. After the first and second blocks, participants were given two practice trials using the on-line feedback.
Data reduction
Surface EMG burst onsets were defined as the point at which the
EMG first began a sustained rise above baseline levels. The location
of this point was determined by first displaying the raw EMG pattern
on a computer monitor with a superimposed line indicating the point
at which activity increased to more than 2 SDs above baseline (mean
of 200 ms of EMG activity preceding movement). Onset was then
verified by visually locating and manually adjusting the onset mark to
the point at which the activity first increased. This method allowed for
correction of errors due to the strictness of the algorithm.
Peak EMG amplitudes were defined as the largest EMG amplitude,
rectified and filtered with a 25-Hz low-pass elliptic filter, recorded
within an interval of 100 ms following EMG burst onset. For each
participant, mean peak EMG amplitudes for the five probe conditions
were expressed as a percentage of the mean peak EMG amplitude for
the control condition. A short time window of 400 ms (from 100 to
500 ms following the probe) was also examined for differences in
angular velocity, since effects of the probe would take ⱖ100 ms to
appear and could be corrected quickly.
Statistical analysis
All dependent variables were analyzed using a simple (6 condition)
repeated measures ANOVA to determine whether differences existed
between control and probe trials. Differences with a P value of ⬍0.05
were considered significant. Dunnett’s and Tukey Honestly Significant Difference post hoc tests were administered to determine the
nature of these differences.
RESULTS
Evidence of a startle response
Table 1 shows the mean onset latencies for the OOc and
SCM muscles for each condition following the presentation of
the stimulus. The onset latencies of SCM were significantly
shorter in all ST trials compared with NST trials (P ⬍ 0.001).
Significant differences also existed in peak EMG amplitude for
SCM between the conditions (F(5, 60) ⫽ 16.75, P ⫽ 0.001;
Fig. 1). Post hoc analysis revealed that SCM peak amplitude in
all three ST conditions, while not being significantly different
from each other, was significantly larger than in Control and
NST conditions (P ⬍ 0.05). Eyeblink (OOc) activity occurred
in both ST and NST trials with no significant difference in
onset latency.
Task accuracy
Participants were successful in accurately performing the
hand-opening task at the correct target angle and accurately
extending the elbow at the correct angular velocity in the
Control condition (see Table 2; see also Fig. 2 Control). SigTABLE
FIG. 1. Mean peak sternocleidomastoid amplitude and SDs. Values for
each condition are expressed as a percentage of the mean peak amplitude for
the Control condition.
nificant differences were found in the onset angle of the secondary movement depending on the condition (F(5, 60) ⫽
7.377, P ⬍ 0.001). Post hoc analysis revealed that hand opening occurred significantly earlier in ST45 trials and significantly later in ST25 trials compared with the Control condition
(P ⬍ 0.05), indicating that the startle differentially affected the
secondary movement depending on the location of the probe.
Analysis of mean angular velocity also revealed differences
between the conditions. Mean angular velocities for the entire
trial (movement onset to hand opening) were significantly
larger in the ST5 and ST25 conditions than in the Control
condition (F(5, 60) ⫽ 15.150, P ⬍ 0.001). However, these
differences in velocity were relatively small in comparison to
differences to angular velocity during a short time window
(400 ms) following the probe (see Table 2). Much larger
differences existed in the mean angular velocities during this
short time period (F(5, 60) ⫽ 11.133, P ⬍ 0.001; Table 2).
Post hoc analysis showed that it was the mean angular velocities for 400 ms following the probe in the ST25 and ST45
conditions that were significantly larger than comparable epochs during Control trials (P ⬍ 0.05), indicating that the startle
affected the ongoing extension movement (see Fig. 2). Mean
angular velocity during the 400-ms window in the ST5 condition, although not significantly different at the P ⫽ 0.05 level,
was also larger than in the Control trials.
EMG data
Analysis of surface EMG data for EDL indicated that differences existed in both the timing and magnitude of the EDL
response (related to hand opening) across conditions (see Table
3 and Fig. 3). The angle at which EDL onset occurred was
found to be different between the conditions (F(5, 60) ⫽ 9.797,
P ⬍ 0.001; Table 3). Post hoc tests revealed that EDL onset
occurred at a significantly smaller amount of extension in ST45
trials and at a significantly larger amount in ST25 trials com-
1. EMG onset latencies for orbicularis oculi and sternocleidomastoid muscles following the stimulus
Muscle
NST25
NST45
ST5
ST25
ST45
Orbicularis oculi (ms)
Sternocleidomastoid (ms)
53.4 ⫾ 12.9
160.9 ⫾ 82.7
63.0 ⫾ 48.4
173.3 ⫾ 106.6
50.5 ⫾ 25.1
71.7 ⫾ 43.6
43.7 ⫾ 11.5
59.3 ⫾ 32.5
44.7 ⫾ 15.4
59.3 ⫾ 24.9
Values are mean ⫾ SD grand values of all participants. EMG, electromyographic; NST, nonstartle trial; ST, startle trial.
J Neurophysiol • VOL
89 • APRIL 2003 •
www.jn.org
1860
TABLE
CARLSEN, HUNT, INGLIS, SANDERSON, AND CHUA
2. Task kinematic data
OA Range
OA SD range
Condition
OA, °
Minimum
Maximum
Minimum
Maximum
Angular Velocity, °/s
Window Velocity, °/s
Control
NST25
NST45
ST5
ST25
ST45
54.88 ⫾ 1.19
54.66 ⫾ 1.41
53.26 ⫾ 1.84
56.34 ⫾ 2.67
57.85 ⫾ 4.42
51.98 ⫾ 3.55
53.29
52.54
49.74
52.10
52.35
47.90
57.37
56.49
56.81
62.99
67.31
61.01
2.41
1.73
2.65
0.47
1.06
0.64
5.03
4.47
6.91
4.08
5.80
6.20
19.69 ⫾ 1.04
19.99 ⫾ 1.20
19.94 ⫾ 1.83
23.74 ⫾ 3.12
23.38 ⫾ 2.18
20.27 ⫾ 1.32
20.81 ⫾ 1.78
23.57 ⫾ 2.76
22.83 ⫾ 11.27
29.98 ⫾ 6.79
43.73 ⫾ 12.30
32.51 ⫾ 18.95
Values are ⫾ SD grand values of all participants. Angular velocity refers to the mean angular velocity observed for the duration of the movement. Window
velocity refers to angular velocity recorded for a 400-ms time window from 100 to 500 ms following the probe stimulus. For the control condition mean values
for comparable time windows were calculated. OA, opening angle. For other abbreviations, see Table 1.
pared with Control trials (P ⬍ 0.05). Significant differences
were also exhibited in the time from displacement onset to
EDL muscle onset (F(5, 60) ⫽ 14.437, P ⬍ 0.001; Table 3).
Time to EDL onset was significantly shorter in all ST trials
(P ⬍ 0.05) compared with Control trials, while no differences
existed between Control trials and NST trials.
Although EDL peak EMG amplitude analysis revealed differences between the conditions (F(5, 60) ⫽ 3.265, P ⫽
0.021), post hoc tests showed that EMG amplitude was only
significantly larger than Control amplitude in the ST45 condition (P ⬍ 0.05; Fig. 3). Analysis of peak EMG amplitude for
TRI also revealed differences between the conditions (F(5,
60) ⫽ 7.522, P ⫽ 0.008). Post hoc tests showed that TRI peak
EMG amplitude was larger in both the ST25 and ST45 conditions than in Control trials (P ⬍ 0.05). Peak TRI amplitude in
the ST5 condition was also larger than Control amplitude,
although not sufficiently large to achieve statistical significance
(Fig. 3).
DISCUSSION
Previous studies involving a “triggering effect” of a startle
on a prepared movement have involved ballistic RT tasks
(Carlsen et al. 2000; Siegmund et al. 2001; Valls-Solé et al.
1995, 1999). In the present study we examined the effect of a
startling stimulus on the secondary component of a compound
movement task. Our findings showed that a startle cannot only
be used to probe response preparation in RT tasks, but also in
an ongoing task (i.e., non-RT task). Furthermore, our findings
revealed that the secondary component of the task (hand opening) was not prepared prior to task initiation but was prepared
and “loaded” on-line, during execution of the primary component of the task (arm extension). Thus, although proprioceptive
information was used successfully to execute the secondary
movement under normal conditions, when the participant was
startled late in the primary movement, the startle was effective
in overriding the kinesthetic coding and inappropriately triggering the secondary movement.
This experiment built on the work of Cordo (1990), Cordo et
al. (1994), and Bevan et al. (1994) by further describing the
nature of compound movements that involve proprioceptive
triggering. This approach was also novel since it was unknown
whether the secondary movement was prepared along with the
primary movement in advance of any movement or whether the
secondary movement was prepared on-line during the execution of the primary movement. In addition, using the startle to
trigger the secondary movement without the involvement of
J Neurophysiol • VOL
the CNS allowed the identification of the epoch in which the
secondary movement was prepared. Similarly, this approach
allowed us to test the hypothesis that the secondary movement,
once prepared, was stored in lower brain structures.
The task
The experimental task was for participants to perform an
active elbow extension movement at a constant rate of 22°/s
coupled with an active hand opening at a prescribed target joint
angle without the use of visual feedback pertaining to joint
position. Consistent with data from Cordo et al. (1994), participants were successful in performing the secondary task
(hand opening) at the target angle. Findings from the present
study showed that, in Control trials, participants performed the
hand opening task with a mean error of only 0.12°, while 67%
of trials had an opening angle within 1.19° of the target (for the
range of opening angle values see Table 1).
Evidence has previously been provided by Cordo et al.
(1994) in support of the notion that participants in their studies
used proprioceptive information regarding elbow joint position
to trigger the execution of the secondary task, rather than a
timing strategy involving time-to-target. Evidence for a timing
strategy in the present experiment would be in the form of
consistent times between conditions from movement onset to
hand opening. Figure 2 and Tables 2 and 3 include data that
would not support the notion of a timing strategy. Although
hand opening occurred at similar joint angles across conditions, the time to hand opening and EDL onset were different.
For example, although in both the Control condition and the
ST5 condition hand opening accuracy was very high (Table 2),
the time-to-target intervals in these conditions were very different (Table 3), indicating that timing was not used to trigger
hand opening. Hand opening in ST trials occurred earlier than
other trials, owing to increased movement velocity in these
trials. For example, in the ST25 condition, if the participant
had used a timing strategy based on the early part of the elbow
trajectory, hand opening would have occurred much later than
observed (see Fig. 2, ST25 dotted line).
Further evidence that participants used a timing strategy
would also be expressed in the form of low variability in mean
angular velocity across trials. This was not seen in Control
trials, as the SD of angular velocity was 1.04°/s (Table 2). At
a constant rate of 22°/s, a 55° elbow extension would take 2.5 s
to complete. The angular velocity variability of 1.04°/s would
therefore manifest itself in a targeting SD of 2.6° over a 2.5-s
time interval. This is much higher than the 1.19° SD exhibited
89 • APRIL 2003 •
www.jn.org
ALTERED TRIGGERING BY STARTLE
1861
FIG. 2. Individual participant sample data. Each box contains sample elbow angle displacement and triceps raw electromyographic (EMG) data over the entire course of a single 4-s trial for each condition. Dashed horizontal line represents the target angle
(55°) while the vertical lines represent probe stimulus presentation (left line) and actual hand opening (right line). Graph for the
Control condition shows only 1 vertical line (hand opening) since no probe occurred. In the ST45 condition the initial trajectory
of the arm is continued predicting the unperturbed movement (dotted line). ST, startle trial; NST, nonstartle trial.
TABLE
3. EDL EMG onset data
Condition
Elbow angle, °
Time, ms
Control
NST25
NST45
ST5
ST25
ST45
53.02 ⫾ 1.04
52.64 ⫾ 1.44
51.02 ⫾ 2.02
54.41 ⫾ 2.74
55.91 ⫾ 4.36
49.09 ⫾ 3.63
2,742.68 ⫾ 147.31
2,694.89 ⫾ 137.47
2,612.92 ⫾ 228.90
2,337.72 ⫾ 285.78
2,400.03 ⫾ 196.36
2,514.20 ⫾ 209.85
Values are ⫾ SD grand values of all participants. Time refers to amount of
time after displacement onset that EDL onset was observed. EDL, extensor
digitorum longus. For other abbreviations, see Table 1.
J Neurophysiol • VOL
by participants in Control trials in the present experiment. Thus
it was concluded that participants were not simply using a
timing strategy of opening the hand 2.5 s into the movement
and suggests that the assertion by Cordo et al. (1994) that
participants used kinesthetic feedback information to trigger
the hand opening was correct.
Effects of the startling stimulus
EMG data from the OOc and SCM were analyzed for
evidence that a startle response was elicited due to the presence
of a startling stimulus. These indicators have been used extensively in other studies involving a startle response (Brown et al.
89 • APRIL 2003 •
www.jn.org
1862
CARLSEN, HUNT, INGLIS, SANDERSON, AND CHUA
FIG. 3. Mean peak EMG amplitudes for extensor digitorum longus (open
squares) and triceps (solid squares). Peak EMG amplitudes in each condition
expressed as a percentage of mean control amplitude for each muscle.
1991; Carlsen et al. 2000; Siegmund et al. 2001). Analysis
revealed that, although the latency of OOc activity (see Table
1) observed in the ST trials was similar to that previously
observed by Brown et al. (1991) in response to a startle (36.7
ms), it was also observed at similar latencies in the NST trials
(see Table 1). In contrast, SCM activity was present at shorter
latencies and larger amplitudes in the ST trials compared with
NST trials (see Table 1), suggesting that the responses to the
two stimuli were different. Furthermore, since the latency of
the SCM was similar to that described previously (58.3 ms) by
Brown et al. (1991), we are satisfied that a startle response was
elicited in the ST trials and not in the NST trials. The occurrence of a startle in the present study resulted in several effects.
One of these effects was that the secondary movement was
elicited early in the ST45 trials. On average, the hand was
opened 3.2° before the target when participants were startled
late in the primary movement. This resulted because, in the
ST45 trials, EDL muscle activity occurred 5.99° prior to the
target. In comparison, in Control trials, EDL onset occurred
only 2.00° prior to the target. We assert that, in the ST45
condition, the startling stimulus triggered the secondary movement. It has been shown previously that startle-evoked EMG
activity in the forearm extensors occurs with a median latency
of approximately 73 ms (Brown et al. 1991). In the present
study, EMG onset in the EDL muscle resulting in the secondary movement occurred at a similarly short latency (median
latency of 82.3 ms) following the presentation of the startling
stimulus. Thus it appears that, rather than being initiated normally by the CNS, the secondary movement was elicited early
by the startle.
Under normal conditions in discrete movement sequences,
proprioceptive information from Ia and II afferents, in the form
of velocity and positional information, can be used by the CNS
to determine when to trigger the secondary movement (Cordo
et al. 1994). Results from experiments by Valls-Solé et al.
(1999), Carlsen et al. (2000), and Siegmund et al. (2001),
however, indicated that prepared movements could also be
triggered by the same structures that are activated by the startle
response. In order for this to take place, the motor commands
must have been accessible by or “loaded into” lower structures
in the brain stem and midbrain, such as the reticulospinal
centers, and have been ready to be released. As such, the
J Neurophysiol • VOL
triggering of the secondary movement by the startle in the
present experiment is consistent with previous startle literature.
Because the early elicitation of the secondary movement (observed in the ST45 condition) was not evident in other conditions, this also gives insight into the temporal structuring of
movement preparation for secondary movements based on a
primary movement. Thus results from the present study indicate that the motor program responsible for the execution of the
secondary movement was “loaded” near the end of the primary
elbow extension movement, likely based on the proprioceptive
information processed on-line by the CNS (see Cordo et al.
1994). The startling stimulus evoked the secondary movement
when it was presented 10° prior to the target, but not when
presented 30° or 50° prior to the target, suggesting that the
secondary movement was prepared and loaded between 10 and
30° prior to reaching the target. Based on an average angular
velocity of approximately 22°/s, this corresponds to a temporal
window of between 400 and 1,500 ms prior to the target. It should
be noted that the 400-ms value is a conservative estimate based on
the task employed and by no means indicates a lower limit on
loading, as it has been previously shown that movement sequences lasting just 210 ms can be coordinated based on proprioceptive information (Cordo et al. 1994). As an alternative hypothesis to late program loading, it may be that the secondary
movement was loaded at the onset of the primary movement but
was not accessible to triggering by a startle stimulus. That is, if the
movement was prepared and loaded at the beginning of the
movement but is only accessible during a certain time window
prior to the target, the same results would be observed.
The hand-opening movement was not evoked by the startling stimulus when it was presented 30° prior to the target
(ST25). In fact, in this condition, hand opening occurred significantly later than in the other conditions (a 2.85° target
overshoot). On average, EDL onset in these trials did not occur
until the target elbow angle had been passed by 0.9°. In the
present study, an increased burst of EMG activity was observed in the TRI during the ongoing extension at a short
latency (median latency of 82 ms) following the startling
stimulus. It has been shown previously that startle-evoked
EMG activity in the TRI occurs with a median latency of
approximately 71 ms (Brown et al. 1991). Since the observed
burst latency value is similar to that reported previously, it
appears as though the EMG in the TRI of the ongoing elbow
extension was facilitated by the startle, possibly by the startle
volley summing with the voluntary EMG activity (see Siegmund et al. 2001). Cordo et al. (1994) showed that, when
participants’ elbows were passively extended, they consistently
overshot the target when elbow joint angular velocity was
unpredictable. They hypothesized that, when velocity information was unreliable, joint position information was used by the
CNS to trigger the secondary movement. However, when triggering was based on positional information, it occurred only
after the target angle had been reached (Cordo et al. 1994). We
assert that EMG facilitation due to the startle resulted in a large
acceleration about the elbow, which would have caused the
angular velocity to become less predictable. An overshoot of
the target occurred during ST25 trials, suggesting that the new
velocity information could not be used in the short amount of
time between the startle and arrival at the target; thus triggering
of the secondary movement was delayed until after the target
had been reached.
89 • APRIL 2003 •
www.jn.org
ALTERED TRIGGERING BY STARTLE
The finding of a target overshoot was unique to ST25 trials.
In the ST5 condition, the participant was startled at the beginning of the elbow extension, allowing more time for a correction in the angular velocity. Thus, as the movement progressed,
the velocity became more predictable, allowing the participant
to execute the hand opening on target. In the ST45 condition,
a large acceleration of the elbow also occurred, resulting in a
change in the angular velocity. However, since the program
responsible for the execution of the hand opening was already
loaded into lower brain structures, it was triggered by the
startle. As such, the hand opening occurred early (prior to
proprioceptive triggering) and thus was independent of the
movement of the arm following presentation of the probe.
EMG activity was increased in both the TRI and EDL as a
result of the startling stimulus and is consistent with previous
literature (Siegmund et al. 2001). Yeomans and Frankland
(1996) suggested that increased amplitude of the startle response was the result of the number of giant neurons recruited
in the reticularis pontis caudalis (RPC) in response to the
startling stimulus. Larger stimulus intensities recruit more RPC
neurons, which may then conduct to the various levels of the
spinal cord, along the reticulospinal tract. If the reticulospinal
tract was an important part of the motor pathway for the task
in the present study, the startle would have acted to facilitate
the ongoing movement at the time of the startle through the
increased activation of the RPC giant neurons. This would
have led to lower recruitment thresholds in the spinal motor
neuron pool and thus to the facilitated movements and movements of higher amplitude exhibited in the present study.
We acknowledge the contributions of I. M. Franks for insight and resources
in the preparation of this manuscript.
This research was supported by a grant from the Natural Sciences and
Engineering Research Council of Canada.
REFERENCES
Bevan L, Cordo P, Carlton L, and Carlton M. Proprioceptive coordination
of movement sequences: discrimination of joint angle versus angular distance. J Neurophysiol 71: 1862–1872, 1994.
J Neurophysiol • VOL
1863
Brown P, Rothwell JC, Thompson PD, Britton TC, Day BL, and Marsden
CD. New observations on the normal auditory startle reflex in man. Brain
114: 1891–1902, 1991.
Carlsen A, Nagelkerke P, Garry M, Hodges N, and Franks IM. Using the
startle paradigm to investigate the nature of a prepared response. J Sport
Exercise Psychol 22S: S24, 2000.
Cordo P, Carlton L, Bevan L, Carlton M, and Kerr GK. Proprioceptive
coordination of movement sequences: role of velocity and position information. J Neurophysiol 71: 1848 –1861, 1994.
Cordo P, Gurfinkel VS, Bevan L, and Kerr GK. Proprioceptive consequences of tendon vibration during movement. J Neurophysiol 74: 1675–
1688, 1995.
Cordo PJ. Kinesthetic control of a multijoint movement sequence. J Neurophysiol 63: 161–171, 1990.
Davis M. The mammalian startle response. In: Neural Mechanisms of Startle
Behavior, edited by RC Eaton. New York: Plenum, 1984, pp. 287–351.
Fischman MG. Programming time as a function of the number of movement
parts and changes in movement direction. J Mot Behav 16: 405– 423, 1984.
Ghez C. Voluntary movement. In: Principles of Neural Science (3rd ed.),
edited by ER Kandel, JH Schwartz, and TM Jessel. New York: Elsevier,
1991, p. 609 – 625.
Keele SW. Movement control in skilled motor performance. Psych Bull 70:
387– 403, 1968.
Scott BW, Frankland PW, Li L, and Yeomans JS. Cochlear and trigeminal
systems contributing to the startle reflex in rats. Neuroscience 91: 1565–
1574, 1999.
Siegmund GP, Inglis JT, and Sanderson DJ. Startle response of human neck
muscles sculpted by readiness to perform ballistic head movements.
J Physiol 535: 289 –300, 2001.
Terzuolo CA and Viviani P. The central representation of learning motor
programs. In: Posture and Movement, edited by RE Talbot and DR Humphrey. New York: Raven Press, 1979.
Valls-Solé J, Rothwell JC, Goulart F, Cossu G, and Muñoz E. Patterned
ballistic movements triggered by a startle in healthy humans. J Physiol 516:
931–938, 1999.
Valls-Solé J, Solé A, Valldeoriola F, Muñoz E, Gonzalez LE, and Tolosa
ES. Reaction time and acoustic startle in normal human subjects. Neurosci
Lett 195: 97–100, 1995.
Wadman WJ, Denier van der Gon JJ, Geuze RH, and Mol CR. Control of
fast goal-directed arm movements. J Hum Mov Stud 5: 3–17, 1979.
Wickens J, Hyland B, and Anson G. Cortical cell assemblies: a possible
mechanism for motor programs. J Mot Behav 26: 66 – 82, 1994.
Yeomans JS and Frankland PW. The acoustic startle reflex: neurons and
connections. Br Res Rev 21: 301–314, 1996.
89 • APRIL 2003 •
www.jn.org