J Neurophysiol 110: 899 –906, 2013.
First published May 29, 2013; doi:10.1152/jn.00065.2013.
Effects of postural threat on spinal stretch reflexes: evidence for increased
muscle spindle sensitivity?
Brian C. Horslen, Chantelle D. Murnaghan, J. Timothy Inglis, Romeo Chua, and Mark G. Carpenter
School of Kinesiology, The University of British Columbia, Vancouver, British Columbia, Canada
Submitted 28 January 2013; accepted in final form 26 May 2013
postural threat; tendon stretch reflex; Hoffmann reflex; arousal; muscle spindle
in which balance is challenged or threatened, they respond by increasing muscle spindle sensitivity to muscle stretch (Prochazka et al. 1985, 1988).
Such changes in muscle spindle sensitivity have been attributed
to an increase in ␥-motoneuron activity to the muscle spindles
(Prochazka et al. 1985, 1988) independent from, or disproportionally to, the amount of ␣-motoneuron activation of extrafusal muscle fibers. Alternatively, mechanisms for increased
muscle spindle sensitivity have been associated with sympathetic arousal (Hunt 1960), possibly through direct links between sympathetic neurons and muscle spindles (Barker and
Saito 1981).
Although early work did not support selective gamma drive
(cf. Gandevia et al. 1997; Gandevia and Burke 1985) or
sympathetic modulation of muscle spindle sensitivity in humans (cf. Macefield et al. 2003), these studies were limited to
WHEN CATS ARE PLACED IN SCENARIOS
Address for reprint requests and other correspondence: M. G. Carpenter,
School of Kinesiology, Univ. of British Columbia, Osborne Centre Unit 1,
6108 Thunderbird Blvd., Vancouver, BC, Canada V6T 1Z4 (e-mail: mark.
[email protected]).
www.jn.org
measuring resting spindle discharge rates in nonstanding tasks,
and typically in unloaded limbs. In contrast, new evidence has
emerged that supports spindle sensitivity changes in humans
within certain behavioral states or when the host muscles are
actively engaged. Recent research has suggested that changes
in muscle spindle sensitivity occur in certain behavioral contexts, such as when people attend to discrete stimuli or engage
in novel tasks. Hospod et al. (2007) and Ribot-Ciscar et al.
(2009) both found that lower-limb muscle spindle firing rates
were increased when subjects had to attend to passive movements compared with when the movements were ignored.
Similarly, Nafati et al. (2004) found that wrist extensor singlemotor unit firing rates were increased in response to tendon
stretch (T) reflexes and decreased with electrically evoked
Hoffmann (H) reflexes when subjects were challenged to make
isometric contractions with high visual feedback gain compared with low gain. Since both reflexes presumably use the
same spinal circuitry yet only T-reflexes directly activate
muscle spindles, it was concluded that the difference was
related to increased spindle sensitivity. Also, Wong et al.
(2011) found that wrist proprioceptive acuity was increased
after learning a new motor task; this was also presumed to be
related to context-specific changes to spindle sensitivity. Functionally, Dimitriou and Edin (2010) have suggested that selective fusimotor drive might indeed be used to uncouple spindle
tension from active muscle contractions to better allow spindles to predict future muscle states. Improving spindle sensitivity might serve to facilitate feedback gain in novel or
attention-demanding situations, better allowing the body to
monitor motor performance.
There is converging evidence to suggest that humans, like
cats, may increase muscle spindle sensitivity when standing or
walking under challenging or threatening conditions. For example, lower-limb ␥-motoneurons can be electrically activated
independently from ␣-motoneurons when subjects are asked to
balance with eyes closed (Aniss et al. 1990) but not when they
are seated (Aniss et al. 1988). T-reflexes have also been shown
to be facilitated when people stand at the edge of an elevated
platform (Davis et al. 2011). Conversely, H-reflexes are found
to be attenuated when people stand on an elevated surface
(Sibley et al. 2007), walk along a narrow elevated beam
(Llewellyn et al. 1990), or balance an inverted pendulum with
their feet (McIlroy et al. 2003). It has been suggested that these
H-reflex changes reflect spinal reflex inhibition, either by
presynaptic mechanisms or homosynaptic postactivation depression, intended to mute the potentially destabilizing effects
of larger stretch reflexes in these scenarios (Llewellyn et al.
1990). While these observations may reflect changes to spindle
sensitivity via either selective gamma drive or sympathetic
0022-3077/13 Copyright © 2013 the American Physiological Society
899
Downloaded from http://jn.physiology.org/ by 10.220.33.4 on June 18, 2017
Horslen BC, Murnaghan CD, Inglis JT, Chua R, Carpenter
MG. Effects of postural threat on spinal stretch reflexes: evidence for
increased muscle spindle sensitivity? J Neurophysiol 110: 899 –906,
2013. First published May 29, 2013; doi:10.1152/jn.00065.2013.—
Standing balance is often threatened in everyday life. These threats
typically involve scenarios in which either the likelihood or the
consequence of falling is higher than normal. When cats are placed in
these scenarios they respond by increasing the sensitivity of muscle
spindles imbedded in the leg muscles, presumably to increase balancerelevant afferent information available to the nervous system. At
present, it is unknown whether humans also respond to such postural
threats by altering muscle spindle sensitivity. Here we present two
studies that probed the effects of postural threat on spinal stretch
reflexes. In study 1 we manipulated the threat associated with an
increased consequence of a fall by having subjects stand at the edge
of an elevated surface (3.2 m). In study 2 we manipulated the threat by
increasing the likelihood of a fall by occasionally tilting the support
surface on which subjects stood. In both scenarios we used Hoffmann
(H) and tendon stretch (T) reflexes to probe the spinal stretch reflex
circuit of the soleus muscle. We observed increased T-reflex amplitudes and unchanged H-reflex amplitudes in both threat scenarios.
These results suggest that the synaptic state of the spinal stretch reflex
is unaffected by postural threat and that therefore the muscle spindles
activated in the T-reflexes must be more sensitive in the threatening
conditions. We propose that this increase in sensitivity may function
to satisfy the conflicting needs to restrict movement with threat, while
maintaining a certain amount of sensory information related to postural control.
900
EFFECTS OF POSTURAL THREAT ON SPINAL STRETCH REFLEXES
METHODS
Ethical Approval
The procedures used in these studies were approved by the University of British Columbia Clinical Research Ethics Board. In study
1, 26 subjects (13 men, 13 women) completed the study, of whom 21
[10 men, 11 women; mean (SD) age ⫽ 22.6 (3.0) yr] met all inclusion
criteria and were included in the final data set. In study 2, 16 male
subjects completed the study [mean (SD) age ⫽ 23.4 (1.23) yr]. No
subjects in either study reported any known neurological, orthopedic,
or vestibular impairment that may have impeded their ability to
complete the study. All subjects gave written informed consent prior
to participation.
Protocol
Postural threat. STUDY 1. A hydraulic lift (Pentalift: M419207B10H01D, Guelph, ON, Canada) was used to manipulate postural
threat. Subjects stood in two threat conditions: a low-threat (LOW)
condition in which they stood 0.8 m above ground and 0.6 m from the
edge of the support surface and a high-threat (HIGH) condition in
which they stood 3.2 m above ground and at the edge of the support
surface. Subjects stood in the same place on the lift in both threat
conditions, and a 0.6-m-wide table was used to extend the support
surface in the LOW condition. Since height-induced postural threat is
known to induce both posterior leaning and changes in background
muscle activity (Carpenter et al. 2001), and since both of these factors
can change H-reflex amplitudes (leaning: Tokuno et al. 2007, 2008,
2009; background activity: Stein et al. 2007), custom-made ankle
braces were used to limit leaning about the ankles and keep background muscle activity constant across conditions. As there are
documented order effects of height-induced postural threat (Adkin et
al. 2000), all subjects experienced the LOW condition first in order to
maximize threat effects.
STUDY 2. For all trials subjects stood on a custom-made servocontrolled tilting platform that could be used to induce both toes-up
and toes-down sagittal-plane perturbations via support surface rotations (amplitude: 7°, duration: 140 ms, angular speed: 50°/s). Threat
of perturbation was manipulated by explicitly informing the subject
whether or not he would be perturbed in the upcoming trial (threat of
perturbation: PRESENT or ABSENT). Instructions were always congruent with the actual platform movement; no perturbations were
experienced in ABSENT trials, while 10 perturbations (5 in each
direction) were presented in a randomized order in PRESENT trials,
such that direction and timing were not predictable.
Since braces would hinder subjects’ ability to recover from the
perturbations, ankle angle was instead monitored online to ensure that
stimuli were presented at consistent angles. Infrared light-emitting
diodes were placed on the fifth metatarsal, lateral malleolus, and tibial
head of the right leg and used to define foot and shank segments, from
which relative angles were calculated (Optotrak Certus, NDI; sampled
at 3,000 Hz). Subjects completed a 60-s quiet standing trial before the
first experimental trial, the data from which were used to set mean ⫾
2 SD stimulation ankle angle windows for both the frontal and sagittal
planes. An experimenter monitored these angles and only evoked
stimuli (H-reflexes, T-reflexes, and perturbations) when subjects were
within these windows. If subjects strayed from the defined bounds,
they were given verbal feedback to guide them back and then stimuli
were presented again once the subject had remained within bounds for
a few seconds.
Arousal manipulation. Affective pictures from the International
Affective Picture System (IAPS) database were used to manipulate
arousal in study 2. Normative IAPS valence (pleasantness) and arousal
(sometimes called intensity) values were used to select pictures to
create two picture groups with similar valence scores yet rated as
either arousing (high arousal) or calming (low arousal). Only pleasant
pictures were used in this study, as they have been previously
demonstrated to cause a greater change in T-reflex amplitudes across
arousal levels than neutral or unpleasant pictures (Bonnet et al. 1995).
Pictures were displayed continuously on a 1 ⫻ 1.3-m screen, 3.7 m in
front of the subject, throughout the trials, and each picture was
displayed for 10 s. No affective pictures were used in study 1.
Reflex stimulation. H-reflexes were elicited in the right soleus
muscle (SOL) with 1-ms-long square-wave electrical pulses to the
tibial nerve at the popliteal fossa (Grass S48 Stimulator, SIU5 Stimulation Isolation Unit, CCU1 Constant Current Unit; Grass Technologies). Prior to commencement of the study an M-wave recruitment
curve was performed for each subject while he/she stood at the LOW
position. These data were used to set the H-reflex stimulation intensity
between 10% and 15% of maximum M-wave amplitude (Mmax).
H-reflexes were elicited in pairs spaced 200 ms apart to induce
J Neurophysiol • doi:10.1152/jn.00065.2013 • www.jn.org
Downloaded from http://jn.physiology.org/ by 10.220.33.4 on June 18, 2017
drive, none of the studies measured both H-reflexes and T-reflexes simultaneously to establish that these effects are occurring concurrently. As such, while the reflex changes reported
across studies seem indicative of a common neurophysiological phenomenon activated under conditions of postural threat,
the studies themselves are too different to aggregate. Therefore, the purpose of this study was to explore the effects of a
postural threat on both H-reflexes and T-reflexes, within the
same subjects, to determine whether spinal stretch reflexes are
indeed altered in a manner consistent with increased muscle
spindle sensitivity.
We adopted two separate postural threat paradigms to explore the effects of threat on spinal reflexes. In study 1, we used
a platform elevated to 3.2 m to increase postural threat by
increasing the consequences of a fall (from height), thus
replicating the type of threat used by both Sibley et al. (2007)
and Davis et al. (2011). In study 2, we used impending balance
perturbations to manipulate postural threat by increasing the
likelihood of a balance disturbance. This paradigm allowed us
to avoid some of the postural changes associated with standing
at height, such as backward leaning and increased muscle
activity related to sway stiffness (Carpenter et al. 1999, 2001;
Davis et al. 2009), that may alter reflex responses if not
controlled (Stein et al. 2007; Tokuno et al. 2007, 2008, 2009).
In addition, this scenario may also be more generalizable to the
types of postural threat experienced in everyday life. We
predicted that in both postural threat scenarios we would see
evidence of increased muscle spindle sensitivity and central
inhibition, as evidenced by increased T-reflexes and decreased
H-reflexes when the postural threat was present.
While postural threat is known to influence fear, anxiety, and
balance confidence, it also induces strong increases in autonomic arousal (Brown et al. 2006; Carpenter et al. 2006; Davis
et al. 2009; Huffman et al. 2009), which by itself can influence
T-reflexes in seated individuals (Bonnet et al. 1995; Both et al.
2005; Hjortskov et al. 2005; Kamibayashi et al. 2009). As such,
a secondary objective in study 2 was determining the effect of
arousal in mediating reflex changes related to postural threat by
exposing subjects to arousing, non-posturally relevant stimuli.
We had subjects watch affective pictures that were specifically
chosen to either promote or reduce arousal. This enabled us to
determine whether arousal alone could influence spindle sensitivity in quiet stance, and whether the effects of threat on
reflexes could be scaled to underlying arousal levels. We
hypothesized that if the reflex changes induced by postural
threat were purely arousal driven, then we would see scaled
reflex changes dependent on both the presence of a postural
threat and either arousing or calming pictures.
EFFECTS OF POSTURAL THREAT ON SPINAL STRETCH REFLEXES
Psychological and autonomic state. Prior to each trial, participants
reported their confidence that they could maintain their balance for the
duration of the trial (0%: not at all confident, 100%: completely
confident). After each trial participants rated their experienced fear of
falling (0%: not at all fearful, 100%: extremely fearful) and anxiety
(16-item questionnaire with a maximum cumulative score of 144,
where higher scores indicate more anxiety). The above questionnaires
were each modified from those used by Adkin et al. (2002) and have
been demonstrated to have moderate to high reliability (Hauck et al.
2008); the individual questionnaire scores were averaged across trials
within each condition.
STUDY 1. Electrodermal activity (EDA), used to quantify physiological arousal, was recorded from the thenar and hypothenar eminences of the nondominant hand for the duration of each trial (model
2501, CED). These data were sampled at 1,000 Hz and then low-pass
filtered at 5 Hz off-line. A mean value was calculated for the duration
of each 150-s trial, and these values were then averaged within height
conditions.
STUDY 2. Since perturbations are known to induce large transient
increases in skin conductance (Sibley et al. 2008), EDA was not
averaged over the course of the trials in this study. EDA was sampled
for 1 s ending 500 ms prior to each stimulus (perturbation, H-reflex,
or T-reflex), and then all of these samples were averaged within a trial
to give a single value. These values were then used for comparison
between trials. Subjects also completed the Self-Assessment Manikin
(SAM) arousal scale (Bradley and Lang 1994) to rate their perceptions
of how arousing the pictures, as a block, were after each trial.
Statistics
For study 1, within-subjects paired-samples t-tests were used to test for
significant changes across threat conditions (LOW, HIGH) for all variables. For study 2, 2 (threat of perturbation: PRESENT, ABSENT) ⫻ 2
(picture condition: calming, arousing) repeated-measures ANOVAs were
used to test for significant differences between conditions for all variables. In all cases, the criterion for statistical significance was set to ␣ ⫽
0.05; ␩2 (t-tests) and partial ␩2 (␩2p, ANOVAs) were used to calculate
effect sizes. All mean differences (⫾SE) and statistical results for studies
1 and 2 are listed in Table 1.
RESULTS
Measures
Electromyography. EMG was recorded at 3,000 Hz from the right
SOL with a monopolar belly-tendon electrode configuration and
analog band-pass filtered between 10 and 1,000 Hz (Telemyo 2400
RG2, Noraxon) and then A/D sampled at 3,000 Hz (Power 1401,
CED). This monopolar configuration was used to measure both H and
T-reflexes, as recommended by Hadoush et al. (2009). Simultaneously, bipolar belly-belly EMG was recorded at 3,000 Hz from both
the right SOL and tibialis anterior muscle (TA). These data were also
analog filtered (10 to 1,000 Hz), and then A/D sampled at 1,000 Hz;
these data were used to quantify background muscle activity.
Background muscle activity was calculated off-line for both SOL
and TA as the root mean square amplitude of a 100-ms period of EMG
immediately preceding a reflex. These values were then averaged
within each condition. Since it is common for individuals to increase
their background muscle activity when standing at height (study 1;
Carpenter et al. 2001), any single reflex evoked that was preceded by
background EMG in either SOL or TA that was more than twice the
mean amplitude of background activity in the LOW or ABSENT
condition was excluded from the analysis. H-reflexes, M waves, and
T-reflexes were all calculated as peak-to-peak amplitudes from the
belly-tendon SOL EMG trace. Reflexes that passed stimulation intensity screening were then averaged within threat conditions.
Study 1
Subject exclusions. Of the 21 subjects who completed the
study, 20 subjects met the T-reflex and 18 the H-reflex inclusion
criteria; 17 subjects met both. One subject was excluded from the
final EDA analysis because of equipment malfunction.
Reflexes and background muscle activity. There was a significant increase in T-reflex peak-to-peak amplitudes in the
HIGH compared with LOW surface height conditions (Fig. 1
and Fig. 2A). H-reflexes, in contrast, were not significantly
modulated with postural threat (Fig. 1 and Fig. 2A). There were
no systematic effects of surface height on M-wave amplitude
(Fig. 2A) or background EMG in either SOL or TA (Table 1).
Psychological and autonomic state. Subjects felt significantly less confident in their ability to maintain balance in the
HIGH compared with LOW surface height conditions. Subjects also felt significantly more fearful of falling, more anxious, and less stable in the HIGH compared with LOW surface
height conditions. Finally, subjects were more aroused, as
indicated by mean EDA, during the HIGH compared with
LOW surface height conditions (Table 1).
J Neurophysiol • doi:10.1152/jn.00065.2013 • www.jn.org
Downloaded from http://jn.physiology.org/ by 10.220.33.4 on June 18, 2017
homosynaptic postactivation depression. However, the evoked M
waves in the second reflex were highly variable, and, as such, we were
not able to interpret the effects of threat on homosynaptic postactivation depression; these data will not be discussed further. T-reflexes
were evoked in the right SOL with mechanical taps to the Achilles
tendon. A magnetic linear motor (motor: LinMot PS01-23x80, controller: LinMot E2000-AT, software: LinMot v.1.3.12; NTI) aligned
perpendicular to the tendon was used to deliver the taps. The motor
was programmed to stroke out 1 cm in 26 ms and was positioned ⬃0.5
cm from the tendon. The peak strike force of each tap on the tendon
was measured with a force transducer (Isotron Dynamic Force Sensor,
Endevco; A/D sampling: 1,000 Hz) mounted to the linear motor.
These forces were used to ensure consistent T-reflex stimulation
intensity. T-reflexes and H-reflexes were presented in a randomized
order within the same trial; stimuli were separated with a variable
interstimulus interval with a minimum period of 10 s. In study 1,
subjects underwent two 150-s trials at each height condition, in which
they received five H-reflex and five T-reflex stimulations. The data
from these trials were compiled for a total of 10 H reflex and 10
T-reflex stimulations per condition. In study 2, subjects received 15
H-reflex and 15 T-reflex stimulations in the two trials without perturbations and 10 H-reflex and 10 T-reflex stimulations in the two trials
with perturbations. A larger number of stimulations were used in study
2 because pilot testing revealed more within-subject variability in
stimulation intensity. Therefore, the number of stimulations was
increased to improve the likelihood of meeting the inclusion criteria.
There were 10 fewer reflexes evoked in the perturbations PRESENT
trials to allow for the extra time required for the 10 platform perturbations. In all, there were always 30 stimulations (H-reflexes, T-reflexes, or perturbations) in a trial.
Reflex inclusion criteria. H-reflexes were screened post hoc to
ensure that only those evoked with an M wave between 10% and 15%
of Mmax were included in the studies. To be consistent with Sibley et
al. (2007), a minimum of five H-reflexes per threat condition was
required for a subject to be included in the final data set. A similar
screening protocol, based on the methods used by Davis et al. (2011),
was used for T-reflexes. For each trial the range of tap forces was
calculated. A mean ⫾ 2 SD window was then calculated from the trial
with the smallest range. T-reflexes evoked with a tap force outside this
window were excluded post hoc. A minimum of five T-reflexes per
condition was required for a subject to be included in the final data set.
901
902
EFFECTS OF POSTURAL THREAT ON SPINAL STRETCH REFLEXES
Table 1. Summary of statistical test results and mean differences across conditions
Study 1
Variable
T-reflex, mV
H-reflex, mV
M wave, mV
TA background, ␮V
Balance confidence, %
Fear, %
Anxiety (max 144)
EDA, ␮S
SAM arousal
t19 ⫽
P⫽
␩2 ⫽
Mean
t17 ⫽
P⫽
␩2 ⫽
Mean
t17 ⫽
P⫽
␩2 ⫽
Mean
t20 ⫽
P⫽
␩2 ⫽
Mean
t20 ⫽
P⫽
␩2 ⫽
Mean
t20 ⫽
P⫽
␩2 ⫽
Mean
t20 ⫽
P⫽
␩2 ⫽
Mean
t20 ⫽
P⫽
␩2 ⫽
Mean
t19 ⫽
P⫽
␩2 ⫽
Mean
N/A
⌬ (SE)
⌬ (SE)
⌬ (SE)
⌬ (SE)
⌬ (SE)
⌬ (SE)
⌬ (SE)
⌬ (SE)
⌬ (SE)
Threat
ⴚ2.60
0.018
0.262
0.558 (0.215)
1.57
0.135
0.120
⫺0.278 (0.177)
⫺1.51
0.149
0.112
0.0556 (0.127)
0.16
0.877
0.001
0.207 (1.32)
⫺0.02
0.981
⬍0.001
0.0164 (0.689)
3.16
0.005
0.333
ⴚ11.8 (3.73)
ⴚ3.34
0.003
0.358
17.4 (5.19)
ⴚ3.34
0.003
0.358
13.7 (4.11)
ⴚ2.57
0.019
0.258
5.41 (2.10)
Statistic
F1,10 ⫽
P⫽
␩P2 ⫽
Mean ⌬
F1,12 ⫽
P⫽
␩P2 ⫽
Mean ⌬
F1,12 ⫽
P⫽
␩P2 ⫽
Mean ⌬
F1,15 ⫽
P⫽
␩P2 ⫽
Mean ⌬
F1,15 ⫽
P⫽
␩P2 ⫽
Mean ⌬
F1,14 ⫽
P⫽
␩P2 ⫽
Mean ⌬
F1,14 ⫽
P⫽
␩P2 ⫽
Mean ⌬
F1,14 ⫽
P⫽
␩P2 ⫽
Mean ⌬
F1,14 ⫽
P⫽
␩P2 ⫽
Mean ⌬
F1,15 ⫽
P⫽
␩P2 ⫽
Mean ⌬
(SE)
(SE)
(SE)
(SE)
(SE)
(SE)
(SE)
(SE)
(SE)
(SE)
Threat
Pictures
Interaction
7.15
0.023
0.417
0.449 (0.168)
2.07
0.176
0.147
0.165 (0.115)
0.285
0.603
0.023
⫺0.0229 (0.0429)
0.12
0.737
0.008
⫺0.320 (0.935)
1.35
0.263
0.083
2.14 (1.84)
11.9
0.004
0.896
ⴚ17.3 (5.03)
12.3
0.003
0.468
18.2 (5.17)
6.07
0.026
0.288
6.34 (2.58)
25.72
⬍0.001
0.648
5.16 (1.02)
1.521
0.236
0.092
0.281 (0.228)
0.005
0.946
⬍0.001
0.00505 (0.073)
0.973
0.343
0.075
0.138 (0.14)
0.375
0.552
0.030
0.022 (0.036)
2.16
0.162
0.126
1.14 (0.778)
3.47
0.082
0.188
1.72 (0.925)
2.204
0.158
0.285
2.66 (1.79)
6.18
0.026
0.306
6.50 (2.61)
1.365
0.261
0.083
1.66 (1.42)
0.027
0.871
0.002
⫺0.124 (0.75)
113.07
⬍0.001
0.883
3.84 (0.361)
0.926
0.359
0.085
–
3.02
0.108
0.201
–
0.446
0.517
0.036
–
0.63
0.438
0.041
–
0.27
0.612
0.018
–
1.22
0.288
0.178
–
4.707
0.048
0.252
–
0.04
0.845
0.003
–
0.58
0.459
0.04
–
1.05
0.323
0.065
–
Study 1: threat: HIGH-LOW. Study 2: threat: perturbations PRESENT-ABSENT, pictures arousing-calming. SOL, soleus muscle; TA, tibialis anterior muscle;
EDA, electrodermal activity; SAM, Self-Assessment Manikin; N/A, not applicable. Significant values are in boldface.
Study 2
Subject exclusions. Of the 16 subjects who completed the
study, 5 were excluded from the final T-reflex analysis because
of high variability in tendon-tap force across conditions. Three
subjects were excluded from the H-reflex analysis, two subjects because of high M-wave variability and one subject could
not tolerate the H-reflex stimuli. Ten subjects were included in
both the T-reflex and H-reflex analyses. One subject was
excluded from the EDA analysis because of equipment malfunction, and psychological state questionnaire data were not
used from one subject because they did not complete the
questionnaires.
Reflexes and background muscle activity. T-reflex amplitudes were significantly larger when the threat of perturbation
was PRESENT compared with ABSENT (Fig. 1 and Fig. 2A).
There was no significant main effect of picture condition or
interaction between threat of perturbation and picture condition
on T-reflex amplitudes. H-reflexes and M-wave amplitudes
were not significantly influenced by the main effects of threat
of perturbation (Fig. 1 and Fig. 2A) or picture condition or by
their interaction. There were no main effects of threat of
perturbation, picture condition, or interaction effects for either
SOL or TA background EMG (Table 1).
Psychological and autonomic state. Participants were significantly more aroused, as indicated by EDA, when the threat
of perturbation was PRESENT compared with ABSENT.
While subjects rated arousing pictures higher on the SAM
arousal scale than calming pictures, there was no effect of
picture condition on EDA, nor was there an interaction
(Table 1).
Participants felt significantly less confident before and more
anxious after the threat of perturbation PRESENT compared
with ABSENT trials; however, there were no significant main
effects of picture condition or interactions affecting these
variables. There was a significant threat of perturbation ⫻
picture condition interaction on rated fear of falling. While fear
of falling was on average higher when the threat of perturbation was PRESENT compared with ABSENT, there were
J Neurophysiol • doi:10.1152/jn.00065.2013 • www.jn.org
Downloaded from http://jn.physiology.org/ by 10.220.33.4 on June 18, 2017
SOL background, ␮V
Statistic
Study 2
EFFECTS OF POSTURAL THREAT ON SPINAL STRETCH REFLEXES
Study 2
T-reflexes
Study 1
T-reflexes
1 mV
0.5 mV
903
50 ms
50 ms
Height
Perturbations
LOW
ABSENT
HIGH
PRESENT
H-reflexes
2 mV
50 ms
50 ms
differences in the effects of picture arousal levels between
these conditions. Post hoc comparisons revealed that subjects
felt significantly more fearful of falling when exposed to
high-arousal compared with low-arousal pictures when the
threat of perturbation was PRESENT (t14 ⫽ ⫺2.60, P ⫽ 0.021,
␩2 ⫽ 0.326) but not when the threat of perturbation was
ABSENT (t14 ⬍ 0.001, P ⬎ 0.999, ␩2 ⬍ 0.001).
Relationship between T and H-reflexes. We performed a
Pearson product-moment correlation post hoc to determine
whether or not changes in T-reflexes might be related to
changes in H-reflexes. Subjects who had both T and H-reflexes
were included, and data from both studies were combined to
increase the sample size (Fig. 2B; n ⫽ 27). Change values were
calculated to normalize the data; changes were expressed as
percent change from the lowest threat condition (i.e., study 1:
LOW, study 2: ABSENT). There was no relationship (r ⫽
⫺0.0928) between changes in T and H-reflexes.
DISCUSSION
Postural threat posed by the increased consequence (study 1)
or likelihood (study 2) of a fall led to increases in arousal, fear,
and anxiety and decreases in balance confidence. In both cases,
the increased threat was accompanied by a significant increase
in the T-reflex amplitude in SOL. The observation of increased
T-reflex amplitudes when standing on an elevated surface
(study 1) or when expecting a balance perturbation (study 2) is
consistent with prior observations of increased T-reflexes under conditions of increased arousal in subjects who are sitting
(Bonnet et al. 1995; Both et al. 2005; Hjortskov et al. 2005;
Kamibayashi et al. 2009) or are standing on elevated surfaces
(Davis et al. 2011). Our observations are unique in that the
increases in T-reflex amplitude with threat are shown to occur
in a posturally engaged muscle, despite the absence of any
concomitant change in H-reflex amplitude or background
EMG. Taken together, this provides evidence to suggest that
these changes may be occurring through increases in muscle
spindle receptor sensitivity rather than reflex facilitation at the
spinal level during stance.
While we interpret these results as being reflective of increased muscle spindle sensitivity with increased postural
threat, there are certain limitations that must be acknowledged.
First, it has been argued that H-reflexes and T-reflexes are not
directly comparable because 1) H-reflexes indiscriminately
activate all large-diameter Ia and Ib afferents compared with
T-reflexes, which are thought to preferentially activate Ia
afferents, and 2) synchronous H-reflex vs. asynchronous T-reflex afferent volleys mean that the reflexes have different
sensitivities to presynaptic and polysynaptic reflex changes
(Burke et al. 1983). However, while the magnitude of effect of
these different factors may differ between reflexes, the direction of effect should be the same. That is, if presynaptic
inhibition were suppressing H-reflexes, then T-reflexes should
also be suppressed, if not to the same degree. Considering the
fact that there was a highly consistent increase in T-reflexes
between subjects and across studies (in that most subjects
showed increases with threat) and no consistent change in
H-reflexes (there is a near-even distribution of subjects who
demonstrated increases and decreases), we suggest that the
factors that influenced T-reflexes with threat did not affect
H-reflexes.
A second limitation in these studies is that muscle history
effects were not controlled between conditions. Muscle spindle
tension, as indicated by discharge rate, can be tonically increased after isometric contraction of the parent muscle (Gregory et al. 1990; Wilson et al. 1995). This is thought to be
caused by formation of stable intrafusal muscle fiber cross
J Neurophysiol • doi:10.1152/jn.00065.2013 • www.jn.org
Downloaded from http://jn.physiology.org/ by 10.220.33.4 on June 18, 2017
2 mV
H-reflexes
Fig. 1. Two representative subjects’ EMG recordings of T-reflexes (top) and H-reflexes
(bottom) delivered while standing on low and
high heights (study 1, left) or in the presence
and absence of perturbations (study 2, right).
The lower threat (LOW, ABSENT) conditions
are drawn in black and the higher threat
(HIGH, PRESENT) conditions in gray.
904
EFFECTS OF POSTURAL THREAT ON SPINAL STRETCH REFLEXES
A
0.8
Threat Source:
Height (Study 1)
0.6
Perturbation (Study 2)
Mean Difference (mV)
0.4
0.2
0
-0.2
-0.6
-0.8
B
*
n.s.
n.s.
T-reflex
M wave
H-reflex
75
Change H-reflex (%)
50
25
0
-25
r = -0.0927
-50
-75
-50
-25
0
25
50
75
100
Change T-reflex (%)
Fig. 2. A: mean amplitude differences between threat conditions for T reflexes, M
waves, and H reflexes for study 1 (gray circles) and study 2 (black squares).
Differences are calculated as HIGH ⫺ LOW or PRESENT ⫺ ABSENT; as such,
higher values indicate larger amplitudes with threat. Bars represent SE. *Significant at P ⬍ 0.05. n.s., Not statistically different. B: scatterplot of mean differences
of T reflexes (x-axis) against H reflexes (y-axis) for all subjects in whom both T
and H reflexes were elicited (n ⫽ 27; study 1: 17, study 2: 10). Data from both
studies are presented together, and differences are expressed as % change. The %
change values were calculated as follows: study 1: (HIGH ⫺ LOW)/LOW ⫻ 100,
study 2: (PRESENT ⫺ ABSENT)/ABSENT ⫻ 100. Positive values indicate an
increase in amplitude with threat, r value calculated with Pearson’s productmoment correlation.
bridges during the contraction (Gregory et al. 1990), a phenomenon known as intrafusal stiction, and has been reported to
last as long as 4 min in resting human subjects (Wilson et al.
1995). Stiction can increase T-reflex amplitudes and has been
suggested to be a major contributor to T-reflex variability when
J Neurophysiol • doi:10.1152/jn.00065.2013 • www.jn.org
Downloaded from http://jn.physiology.org/ by 10.220.33.4 on June 18, 2017
-0.4
not controlled (Wood et al. 1994). There were no changes in
background muscle activity that would suggest a conditioning
contraction in the threatening conditions of either of our
studies; however, we cannot exclude the possibility that such a
contraction occurred between trials when EMG was not recorded. Despite this, we would argue that stiction effects
cannot explain the results from study 2, as the large-amplitude
stretches and subsequent dynamic contractions associated with
the perturbations in the perturbations PRESENT condition
would have broken the stable cross bridges and reset spindle
tension (Wilson et al. 1995).
The final limitations that must be addressed are the potential
effects of ankle bracing in study 1 and auditory feedback in
study 2. It is possible that the ankle braces used to control
leaning in study 1 provided additional haptic feedback or
changed the locus of postural control from the ankle joints to
the knees. Similarly, the use of occasional auditory feedback to
guide subjects back to a constant ankle angle in study 2 may
have caused subjects to adopt a more conscious control of
posture than usual. While the potential for each of these issues
to influence stretch reflexes is unknown, each limitation applies
to only one study, and therefore it is unlikely that either of
these factors would contribute to reflex changes observed
across both of these studies.
Since we did not observe changes in H-reflexes or background EMG, it could be argued that the changes in spindle
sensitivity occurred without systematic changes in tonic ␣-motoneuron activity, which would suggest ␣-␥ decoupling. Reduced animal preparations have demonstrated that ␥-motoneuron activity can be influenced by reticulospinal and vestibulospinal projections (cf. Hulliger 1984 for review), both of
which are excited in states of fear, anxiety, or arousal (Balaban
2002; Balaban and Thayer 2001). However, direct neural
recordings would be required to confirm this hypothesis. Alternatively, the changes in muscle spindle sensitivity could be
related to the influence of sympathetic neurons acting directly
on muscle spindles (Barker and Saito 1981); sympathetic
nervous system activity was increased in the present studies, as
indicated by increases in EDA (Venables 1991). These findings, along with others, support the hypothesis that arousal
influences muscle spindle sensitivity. Changes in muscle spindle sensitivity have been implicated in increases in Ia afferent
firing rate with a kinesthetic attention task (Hospod et al. 2007;
Ribot-Ciscar et al. 2009) or mental arithmetic (Ribot-Ciscar et
al. 2000). Also, T-reflexes have been shown to be increased
independently from H-reflexes in quiescent SOL with tasks
that increase heart rate and blood pressure, such as mental
arithmetic and isometric handgrip (Kamibayashi et al. 2009).
These studies support the theory that balance-relevant proprioceptive inputs can be modulated to suit changes in postural
context, such as when the eyes are closed (Aniss et al. 1990) or
threat is increased (Davis et al. 2011; Prochazka et al. 1988).
These changes have been proposed as a means of increasing
“feedback gain and resolution” to supraspinal areas in challenging motor tasks (Llewellyn et al. 1990). However, it is not
yet clear which supraspinal centers would use this information,
as Davis et al. (2011) demonstrated that threat-induced increases in T reflexes are not associated with larger somatosensory cortical potentials. Therefore, it is more likely that a
subcortical system uses this increase in afferent information.
EFFECTS OF POSTURAL THREAT ON SPINAL STRETCH REFLEXES
In conclusion, we have demonstrated that postural threat, be
it from increased consequences or likelihood of a fall, leads to
an amplification of tendon stretch reflexes, without any concomitant change in H-reflex amplitude. The most likely explanation for this effect is through an increase in muscle spindle
sensitivity, possibly due to fusimotor drive independent of
tonic changes to muscle activation state, or increases in sympathetic drive. We propose that this increase in sensitivity
might reflect an adaptation strategy meant to satisfy the conflicting needs to restrict movement with threat and to maintain
a certain amount of sensory information related to postural
control. These data further support the notion that sensory
modalities can adapt to different contexts and that automatic
behavioral changes seen with threat may be linked to changes
in sensory monitoring of postural control.
ACKNOWLEDGMENTS
These data have been published in part as a thesis by B. C. Horslen.
GRANTS
The authors thank the Natural Sciences and Engineering Research Council
(NSERC) for financial support.
DISCLOSURES
No conflicts of interest, financial or otherwise, are declared by the author(s).
AUTHOR CONTRIBUTIONS
Author contributions: B.C.H., C.D.M., J.T.I., R.C., and M.G.C. conception
and design of research; B.C.H. and C.D.M. performed experiments; B.C.H.
and C.D.M. analyzed data; B.C.H., C.D.M., J.T.I., R.C., and M.G.C. interpreted results of experiments; B.C.H. prepared figures; B.C.H. drafted manuscript; B.C.H., C.D.M., J.T.I., R.C., and M.G.C. edited and revised manuscript;
B.C.H., C.D.M., J.T.I., R.C., and M.G.C. approved final version of manuscript.
REFERENCES
Adkin AL, Frank JS, Carpenter MG, Peysar GW. Fear of falling modifies
anticipatory postural control. Exp Brain Res 143: 160 –170, 2002.
Adkin AL, Frank JS, Carpenter MG, Peysar GW. Postural control is scaled
to level of postural threat. Gait Posture 12: 87–93, 2000.
Aniss AM, Diener HC, Hore J, Burke D, Gandevia SC. Reflex activation of
muscle spindles in human pretibial muscles during standing. J Neurophysiol
64: 671– 679, 1990.
Aniss AM, Gandevia SC, Burke D. Reflex changes in muscle spindle
discharge during a voluntary contraction. J Neurophysiol 59: 908 –921,
1988.
Balaban CD. Neural substrates linking balance control and anxiety. Physiol
Behav 77: 469 – 475, 2002.
Balaban CD, Thayer JF. Neurological bases for balance-anxiety links. J
Anxiety Disord 15: 53–79, 2001.
Barker D, Saito M. Autonomic innervation of receptors and muscle fibres in
cat skeletal muscle. Proc R Soc Lond B Biol Sci 212: 317–332, 1981.
Bonnet M, Bradley MM, Lang PJ, Requin J. Modulation of spinal reflexes:
arousal, pleasure, action. Psychophysiology 32: 367–372, 1995.
Both S, Boxtel G, Stekelenburg J, Everaerd W, Laan E. Modulation of
spinal reflexes by sexual films of increasing intensity. Psychophysiology 42:
726 –731, 2005.
Bradley MM, Lang PJ. Measuring emotion: the Self-Assessment Manikin
and the Semantic Differential. J Behav Ther Exp Psychiatry 25: 49 –59,
1994.
Brown LA, Polych MA, Doan JB. The effect of anxiety on the regulation of
upright standing among younger and older adults. Gait Posture 24: 397–
405, 2006.
Brown LA, Gage WH, Polych MA, Sleik RJ, Winder TR. Central set
influences on gait. Age-dependent effects of postural threat. Exp Brain Res
145: 286 –296, 2002.
J Neurophysiol • doi:10.1152/jn.00065.2013 • www.jn.org
Downloaded from http://jn.physiology.org/ by 10.220.33.4 on June 18, 2017
If we presume that people use normal postural sway not just
to balance but also to maintain a certain volume or quality of
dynamic sensory input (Carpenter et al. 2010; Murnaghan et al.
2011), then increasing sensitivity of balance-relevant sensory
sources should mean that less body sway would be required to
maintain a requisite volume of sway-generated sensory information. In fact, this is exactly what happens to postural sway
(Carpenter et al. 2001) and center of foot pressure (Carpenter
et al. 1999; Davis et al. 2009) when people stand in high
postural threat scenarios. Likewise, if the volume of sensory
information evoked by a perturbation is larger than normal
under conditions of postural threat, as would be suggested by
an increase in spindle sensitivity, then the postural reaction to
the balance perturbation may also be different from normal.
This might translate into altered postural responses, as observed when perturbations are evoked at different levels of
postural threat (Brown and Frank 1997; Carpenter et al. 2004).
It must be acknowledged that our lack of observed changes in
H-reflex amplitude with threat (studies 1 and 2) differs from those
studies that have reported H-reflex inhibition under conditions of
postural challenge (Llewellyn et al. 1990; McIlroy et al. 2003) or
threat (Sibley et al. 2007). The most likely explanation for the
discrepancy between studies is a difference in the task and/or
level of threat. Llewellyn et al. (1990) observed a decrease in
the peak H-reflex amplitude, primarily in stance phase of the
gait cycle, when subjects walked on a 3.5-cm-wide, 34-cmhigh beam. This observation may be related to changes in gait
parameters, known to occur when walking under conditions of
increased threat (Brown et al. 2002; Caetano et al. 2009;
Tersteeg et al. 2012) as opposed to a direct effect of threat
itself. Likewise, Sibley et al. (2007) had subjects stand on a
platform that was much lower than that used in study 1 (1.6 m
vs. 3.2 m), and they did not restrict leaning or changes in
background EMG, both of which may have potentially influenced their results (Stein et al. 2007; Tokuno et al. 2007, 2008,
2009). Alternatively, the ankle braces used in study 1 may have
provided additional sensory feedback that prevented H-reflex
inhibition that was not available to the subjects in the Sibley et
al. (2007) study. However, the same increase in T-reflexes
without a change in H-reflexes was observed when we removed the braces for study 2, suggesting that the braces did not
contribute to the lack of significant H-reflex changes in these
studies.
It is also notable that we did not replicate the effects of
affective picture-induced arousal on soleus T-reflexes (cf. Bonnet et al. 1995). This is likely due to the fact that we could not
induce a change in arousal, as indicated by EDA, across picture
conditions. While there were differences in subjective ratings
of arousal, these effects did not translate to either EDA or
T-reflexes. The failure to elicit increased EDA is in contrast
with both Bonnet et al. (1995) and previous work from our
research group (Horslen and Carpenter 2011). It is possible that
the arousal evoked by the pictures was not sufficiently strong
to induce an appreciable difference in EDA across picture
conditions on top of the transient changes related to H and
T-reflexes. Postural perturbations are known to evoke transient
increases in EDA, known as electrodermal responses (Sibley et
al. 2008). H and T-reflexes, which cause small postural disturbances and may be somewhat painful, may have overridden
any potential picture effects and may therefore have masked
the potential changes in T-reflexes related to arousing pictures.
905
906
EFFECTS OF POSTURAL THREAT ON SPINAL STRETCH REFLEXES
Kamibayashi K, Nakazawa K, Ogata H, Obata H, Akai M, Shinohara M.
Invariable H-reflex and sustained facilitation of stretch reflex with heightened sympathetic outflow. J Electromyogr Kinesiol 19: 1053–1060, 2009.
Llewellyn M, Yang JF, Prochazka A. Human H-reflexes are smaller in
difficult beam walking than in normal treadmill walking. Exp Brain Res 83:
22–28, 1990.
Macefield VG, Sverrisdottir YB, Wallin BG. Resting discharge of human
muscle spindles is not modulated by increases in sympathetic drive. J
Physiol 551: 1005–1011, 2003.
McIlroy WE, Bishop DC, Staines WR, Nelson AJ, Maki BE, Brooke JD.
Modulation of afferent inflow during the control of balancing tasks using the
lower limbs. Brain Res 961: 73– 80, 2003.
Murnaghan CD, Horslen BC, Inglis JT, Carpenter MG. Exploratory
behavior during stance persists with visual feedback. Neuroscience 195:
54 –59, 2011.
Nafati G, Rossi-Durand C, Schmied A. Proprioceptive control of human
wrist extensor motor units during an attention-demanding task. Brain Res
1018: 208 –220, 2004.
Prochazka A, Hulliger M, Trend P, Durmuller N. Dynamic and static
fusimotor set in various behavioural contexts. In: Mechanoreceptors: Development, Structure, and Function, edited by Hnik P, Soukup T, Vejsada R,
Zelena J. New York: Plenum, 1988, p. 417– 430.
Prochazka A, Hulliger M, Zangger P, Appenteng K. “Fusimotor set”: new
evidence for ␣-independent control of ␥-motoneurones during movement in
the awake cat. Brain Res 339: 136 –140, 1985.
Ribot-Ciscar E, Rossi-Durand C, Roll JP. Increased muscle spindle sensitivity to movement during reinforcement manoeuvres in relaxed human
subjects. J Physiol 523: 271–282, 2000.
Ribot-Ciscar E, Hospod V, Roll J, Aimonetti J. Fusimotor drive may adjust
muscle spindle feedback to task requirements in humans. J Neurophysiol
101: 633– 640, 2009.
Sibley KM, Carpenter MG, Perry JC, Frank JS. Effects of postural anxiety
on the soleus H-reflex. Hum Mov Sci 26: 103–112, 2007.
Sibley KM, Mochizuki G, Esposito JG, Camilleri JM, McIlroy WE. Phasic
electrodermal responses associated with whole-body instability: presence
and influence of expectation. Brain Res 1216: 38 – 45, 2008.
Stein RB, Estabrooks KL, McGie S, Roth MJ, Jones KE. Quantifying the
effects of voluntary contraction and inter-stimulus interval on the human
soleus H-reflex. Exp Brain Res 182: 309 –319, 2007.
Tersteeg MC, Marple-Horvat DE, Loram ID. Cautious gait in relation to
knowledge and vision of height: is altered visual information the dominant
influence? J Neurophysiol 107: 2686 –2691, 2012.
Tokuno CD, Carpenter MG, Thorstensson A, Garland SJ, Cresswell AG.
Control of the triceps surae during the postural sway of quiet standing. Acta
Physiol (Oxf) 191: 229 –236, 2007.
Tokuno CD, Taube W, Cresswell AG. An enhanced level of motor cortical
excitability during the control of human standing. Acta Physiol (Oxf) 195:
385–395, 2009.
Tokuno CD, Garland SJ, Carpenter MG, Thorstensson A, Cresswell AG.
Sway-dependent modulation of the triceps surae H-reflex during standing. J
Appl Physiol 104: 1359 –1365, 2008.
Venables PH. Autonomic activity. Ann NY Acad Sci 620: 191–207, 1991.
Wilson LR, Gandevia SC, Burke D. Increased resting discharge of human
spindle afferents following voluntary contractions. J Physiol 488: 833– 840,
1995.
Wong JD, Wilson ET, Gribble PL. Spatially selective enhancement of
proprioceptive acuity following motor learning. J Neurophysiol 105: 2512–
2521, 2011.
Wood SA, Morgan DL, Gregory JE, Proske U. Fusimotor activity and the
tendon jerk in the anaesthetised cat. Exp Brain Res 98: 101–109, 1994.
J Neurophysiol • doi:10.1152/jn.00065.2013 • www.jn.org
Downloaded from http://jn.physiology.org/ by 10.220.33.4 on June 18, 2017
Brown LA, Frank JS. Postural compensations to the potential consequences
of instability: kinematics. Gait Posture 6: 89 –97, 1997.
Burke D, Gandevia SC, McKeon B. The afferent volleys responsible for
spinal proprioceptive reflexes in man. J Physiol 339: 535–552, 1983.
Caetano MJ, Gobbi LT, Sánchez-Arias MR, Stella F, Gobbi S. Effects of
postural threat on walking features of Parkinson’s disease patients. Neurosci
Lett 452: 136 –140, 2009.
Carpenter MG, Frank JS, Adkin AL, Paton A, Allum JH. Influence of
postural anxiety on postural reactions to multi-directional surface rotations.
J Neurophysiol 92: 3255–3265, 2004.
Carpenter MG, Frank JS, Silcher CP. Surface height effects on postural
control: a hypothesis for a stiffness strategy for stance. J Vestib Res 9:
277–286, 1999.
Carpenter MG, Frank JS, Silcher CP, Peysar GW. The influence of
postural threat on the control of upright stance. Exp Brain Res 138:
210 –218, 2001.
Carpenter MG, Murnaghan CD, Inglis JT. Shifting the balance: evidence of
an exploratory role for postural sway. Neuroscience 171: 196 –204, 2010.
Carpenter MG, Adkin AL, Brawley LR, Frank JS. Postural, physiological
and psychological reactions to challenging balance: does age make a
difference? Age Ageing 35: 298 –303, 2006.
Davis JR, Campbell AD, Adkin AL, Carpenter MG. The relationship
between fear of falling and human postural control. Gait Posture 29:
275–279, 2009.
Davis JR, Horslen BC, Nishikawa K, Fukushima K, Chua R, Inglis JT,
Carpenter MG. Human proprioceptive adaptations during states of heightinduced fear and anxiety. J Neurophysiol 106: 3082–3090, 2011.
Dimitriou M, Edin BB. Human muscle spindles act as forward sensory
models. Curr Biol 20: 1763–1767, 2010.
Gandevia SC, Wilson LR, Inglis JT, Burke D. Mental rehearsal of motor
tasks recruits alpha-motoneurones but fails to recruit human fusimotor
neurones selectively. J Physiol 505: 259 –266, 1997.
Gandevia SC, Burke D. Effect of training on voluntary activation of human
fusimotor neurons. J Neurophysiol 54: 1422–1429, 1985.
Gregory JE, Mark RF, Morgan DL, Patak A, Polus B, Proske U. Effects
of muscle history on the stretch reflex in cat and man. J Physiol 424:
93–107, 1990.
Hadoush H, Tobimatsu Y, Nagatomi A, Kimura H, Ito Y, Maejima H.
Monopolar surface electromyography: a better tool to assess motoneuron
excitability upon passive muscle stretching. J Physiol Sci 59: 243–247,
2009.
Hauck LJ, Carpenter MG, Frank JS. Task-specific measures of balance
efficacy, anxiety, and stability and their relationship to clinical balance
performance. Gait Posture 27: 676 – 682, 2008.
Hjortskov N, Skotte J, Hye-Knudsen C, Fallentin N. Sympathetic outflow
enhances the stretch reflex response in the relaxed soleus muscle in humans.
J Appl Physiol 98: 1366 –1370, 2005.
Horslen BC, Carpenter MG. Arousal, valence and their relative effects on
postural control. Exp Brain Res 215: 27–34, 2011.
Hospod V, Aimonetti J, Roll J, Ribot-Ciscar E. Changes in human muscle
spindle sensitivity during a proprioceptive attention task. J Neurosci 27:
5172–5178, 2007.
Huffman JL, Horslen BC, Carpenter MG, Adkin AL. Does increased
postural threat lead to more conscious control of posture? Gait Posture 30:
528 –532, 2009.
Hulliger M. The mammalian muscle spindle and its central control. Rev
Physiol Biochem Pharmacol 101: 1–110, 1984.
Hunt CC. The effect of sympathetic stimulation on mammalian muscle
spindles. J Physiol 151: 332–341, 1960.