The Effect of Deep and Slow Breathing On Pain Perception, Autonomic Activity, and Mood ProcessingAn Experimental Study
The Effect of Deep and Slow Breathing On Pain Perception, Autonomic Activity, and Mood ProcessingAn Experimental Study
Volker Busch, MD,* Walter Magerl, MD,† Uwe Kern, DSB intervention, subjects were asked to breathe
MD,‡ Joachim Haas, MD,* Göran Hajak, MD,* and guided by a respiratory feedback task requiring a
Peter Eichhammer, MD* high degree of concentration and constant atten-
tion. In the relaxing DSB intervention, the subjects
*Department of Psychiatry and Psychosomatic relaxed during the breathing training. The skin con-
Medicine, University of Regensburg, Regensburg; ductance levels, indicating sympathetic tone, were
measured during the breathing maneuvers. Thermal
†
Department of Neurophysiology, Centre of detection and pain thresholds for cold and hot
stimuli and profile of mood states were examined
Biomedicine and Medical Technology Mannheim
before and after the breathing sessions.
(CBTM), University of Heidelberg, Mannheim;
Results. The mean detection and pain thresholds
‡
Centre for Pain Management & Palliative Care, showed a significant increase resulting from the
Wiesbaden, Germany relaxing DSB, whereas no significant changes of
these thresholds were found associated with the
Reprint requests to: Volker Busch, MD, Center for Pain attentive DSB. The mean skin conductance levels
and Affective Disorders, Department of Psychiatry, indicating sympathetic activity decreased signifi-
Psychotherapy and Psychosomatic Medicine, cantly during the relaxing DSB intervention but not
University of Regensburg, Universitätsstraße 84, during the attentive DSB. Both breathing interven-
93059 Regensburg, Germany. Tel: 49-941-941-0; Fax: tions showed similar reductions in negative feelings
49-941-941-2925; E-mail: [email protected]. (tension, anger, and depression).
Authors Approval/Disclosure: All authors have Conclusion. Our results suggest that the way of
personally reviewed and given final approval of the breathing decisively influences autonomic and pain
version submitted, and neither the manuscript nor its processing, thereby identifying DSB in concert with
data have been previously published or are currently relaxation as the essential feature in the modulation
under consideration of publication. of sympathetic arousal and pain perception.
215
Busch et al.
216
Effect of Breathing on Pain Perception
P P
O Detection and NB Breathing NB Breathing NB Breathing Detection and O
M Pain Thresholds Intervention Intervention Intervention Pain Thresholds M
S (attentive or (attentive or (attentive or S
relaxing DSB) relaxing DSB) relaxing DSB)
Figure 1 Course of the study. Sup. Training = training under supervision; min = minute; POMS = profile of
mood states; DSB = deep and slow breathing; NB = natural breathing.
1. Attentive DSB (aDSB): The subjects were asked to were supervised and guided by a trained biofeedback
breathe according to a respiratory feedback task [33], expert. The subjects were instructed not to hold their
assuming an “externally paced” respiration with the breath, but to breathe slowly and deeply throughout the
help of a given ideal breathing curve representing res- breathing cycle. In both interventions, expiratory/
piration frequency and depth. The ideal breathing curve inspiratory time ratio of each breathing cycle was 60/30%,
and the individual breathing curve were presented followed by a brief pause (10%), similar to the recommen-
together on a monitor. The subjects had to try to fit their dation for DSB in literature [16,38]. To control for interac-
own respiration curve to the ideal curve, which required tion effects between the experimenter and the participant
constant attention and concentration on the breathing and in order to get similar breathing depths and rates, the
task. experimenter provided similar breathing instructions and
2. Relaxing DSB (rDSB): The subjects were told to direct supported the participants by giving the same number of
their awareness on the experience of breathing. They directly addressed verbal suggestions in both groups.
had to look on a spot on a wall with their eyes kept Structured sentences were based upon voice dialogue
open. They were “internally paced” by verbal instruc- recommendations used in deep relaxing breathing therapy
tions of the experimenter in order to provide similar regimens [39]. Total duration of the breathing training in
respiration rates and depths compared with the aDSB each microcycle was 20 minutes, consisting of one base-
intervention. The subjects did not get a visual control of line period of 2–3 minutes, followed by three breathing
their performance, as their breathing activities were not blocks of 5 minutes (interrupted each by short breaks of 1
fed back on a monitor. These aspects provided a type minute). The baseline period served as an adaptation
of breathing that required very little cognitive process- phase to get accustomed to the laboratory situation and
ing and which has been reported to induce a more to allow the experimenter to calibrate the equipment.
meditative state [7,34–36]. Values from baseline and breathing breaks were not used
for further analyses.
In both interventions, the subjects were instructed to keep
a constant, slow, and deep diaphragmal breathing rhythm Measurement of Breathing Parameters
with a respiration rate of 7 cpm (cycles per minute), which
is approximately half of the normal rate, that had been Breathing techniques used in biofeedback and voluntary
recommended in previous studies investigating the effects breathing training paradigms are often designed to control
of DSB on arousal [37]. Furthermore, a respiration depth for thoracic or abdominal respiration movements [40]. In
of 2 cm amplitude/cycle was required. Both interventions studies of voluntarily controlling of breathing activity, the
217
Busch et al.
abdominal control of respiration—with and without visual the breathing training was performed six times in
control—accurately reproduced specified breathing fre- each mesocycle under supervision of the trainer (once
quencies and depths [41]. Therefore, we used an abdomi- per week), the thermal detection and pain thre-
nal respiratory module fixed around the subject’s upper sholds only from the first, fourth, and sixth microcycles
abdomen using a strain gauge belt. To ensure the same were measured, each before and after the breathing
and correct position, the device was mounted 5 cm above intervention.
the umbilicus, directly on the skin. The module was a
two-channel device (resolution 0.2 mm, measurement Measurement of Sympathetic Activity
range 20 cm) producing a digitalized signal of the ana-
logue respiration movements (amplitude in mm/cycle, fre- The skin conductance level (SCL) represents the electrical
quency in cpm). The respiration rates and depths from all conductance of the skin, which varies with its moisture
three blocks of one microcycle and then from the first, level. Any changes in eccrine sweating are related to
218
Effect of Breathing on Pain Perception
physiological response to stress [61,62]. Room tempera- score of the final sample for BDI was 4.27 (⫾3.24), which
ture was kept stable at 20°C [63]. As many substances is significantly below the cutoff of 18 points indicating a
can affect the sympathetic activity measured by SCL, depressive disorder [25]. The mean score of the final
subjects were asked to refrain from drinking alcohol for at sample for anxiety (trait) was 38.70 (⫾8.80), well within the
least 48 hours, from drinking more than two cups of coffee 95% confidence interval for male and female adoles-
on the day of the measurement, and from smoking for at cents (age 15–29; 34.49 ⫾ 5.5 female adolescents,
least 2 hours before the recording [64,65]. The subjects 35.65 ⫾ 5.7 male adolescents) [30]. All remaining sub-
were encouraged to sit comfortably in a chair and rest jects (13 female adolescents, 2 male adolescents) accom-
their hands on their laps. plished both mesocycles of the study. None of the
subjects reported any undesirable side effects.
Statistics
Data Distribution
aDSB rDSB
M ⫾ SD M ⫾ SD T P
Respiration depths (cm) Baseline 0.95 ⫾ 0.50 1.01 ⫾ 0.37 -0.45 ns (0.66)
Breathing blocks 2.25 ⫾ 0.70 2.02 ⫾ 0.77 1.53 ns (0.15)
Breaks 0.98 ⫾ 0.43 0.95 ⫾ 0.40 0.52 ns (0.61)
Respiration rates (min-1) Baseline 15.05 ⫾ 2.04 14.16 ⫾ 2.54 1.29 ns (0.22)
Breathing blocks 7.04 ⫾ 0.52 7.65 ⫾ 1.26 -1.10 ns (0.29)
Breaks 15.77 ⫾ 2.59 14.45 ⫾ 2.57 1.85 ns (0.09)
Comparison of the mean (⫾SD) respiration depths and rates for the baseline period, all breathing blocks, and breaks of the first,
fourth, and sixth microcycles in the aDSB and rDSB intervention.
aDSB = attentive deep and slow breathing; rDSB = relaxing deep and slow breathing; M = mean; SD = standard deviation;
T = paired test statistic; P = Significance; ns = nonsignificant.
219
Busch et al.
aDSB = attentive deep and slow breathing; rDSB = relaxing deep and slow breathing; CDT = cold detection threshold; WDT = warm detection threshold; CPT = cold pain threshold;
(⫾2.87)
(⫾3.35)
(⫾3.22)
(⫾4.04)
(⫾3.72)
(⫾3.39)
factor “session” and the interaction of “intervention*
M (⫾SD)
session” for both detection and pain thresholds. The
factor “course” and its interactions did not explain a
37.86
39.67
40.19
39.76
41.36
40.23
Detection and pain thresholds of the first, fourth, and sixth microcycles before (pre) and after (post) the breathing maneuvers in the aDSB and rDSB intervention (in °C).
Post significant portion of variance in this model (Table 3). Post
hoc analyses allocated the overall increase of pain (-0.27,
P = < 0.001, Cohen’s d = 1.01) as well as detection (0.73,
(⫾2.97) P = < 0.001; Cohen’s d = 0.88) thresholds under the con-
(⫾3.41)
(⫾4.13)
(⫾3.71)
(⫾3.79)
(⫾4.12)
dition of the rDSB, whereas no change of the overall pain
M (⫾SD)
HPT = heat pain threshold; SD = standard deviation; M = mean; SD = standard deviation; M1 = microcycle 1; M4 = microcycle 4, M6 = microcycle 6.
Pre
(⫾5.67)
(⫾2.99)
(⫾4.62)
(⫾3.89)
(⫾5.11)
Pre
(Figure 2).
Correlation Analyses
(⫾0.52)
(⫾0.95)
(⫾0.54)
(⫾0.60)
(⫾0.53)
(⫾0.54)
with regard to the rDSB (r = -0.40; P < 0.05) but not to the
Post
33.51
33.22
33.64
33.35
33.41
33.55
WDT
30.96
30.74
30.18
30.43
30.08
30.01
Post
Discussion
M (⫾SD)
31.03
30.74
30.40
30.97
30.70
30.69
CDT
aDSB
rDSB
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Effect of Breathing on Pain Perception
Table 3 ANOVA for repeated measurements for detection and pain thresholds
Analyses of variance for repeated measurements for z-transformed detection and pain thresholds. Main effects and interactions are
shown for a three-factorial model with “intervention” (attentive deep and slow breathing vs relaxing deep and slow breathing),
“course” (microcycle 1 vs microcycle 4 vs microcycle 6), and “session” (before vs after a breathing training) as within subject factors.
ANOVA = analysis of variance; F = ANOVA test statistic; P = significance; df = degrees of freedom of hypothesis and error;
ns = nonsignificant. Bold denotes significant results.
aDSB associated with a concentration task requiring per- in a psychomotor task motor speed [71] and psychomotor
sistent attentional focusing, whereas in the other interven- vigilance was even improved, even in novice meditators
tion, a DSB mode particularly aiming at pure relaxation [72].
without mental effort was chosen.
One could argue that the subjects may not be distracted
The most striking finding in the present study was a sig- equally during both interventions and that a different
nificant increase of pain thresholds in our subjects only amount of distraction between both groups may have
after the rDSB condition in all of the three microcycles, additionally contributed to the effects of the breathing
thereby indicating an attenuation of pain perception trainings on detection and pain thresholds. However, we
(becoming less sensitive). In contrast, the aDSB mode did take the view that distraction may not significantly sepa-
not alter pain and detection thresholds. rate both interventions, as some of the subjects may be
more distracted by fitting their respiration curve onto an
In keeping with our findings of increased pain thresholds ideal curve during the first intervention; some others may
after the rDSB, recent work underscores the potential be similarly distracted by dwelling on thoughts during the
utility of a DSB training in reducing pain intensity ratings second intervention.
as compared with a natural or rapid breathing mode
[14,18,68]. Intriguingly, due to the study design, the afore- Interestingly, detection as well as pain thresholds
mentioned investigations could not differentiate between increased following the rDSB, suggesting that this type of
the effect of relaxation and the effect of respiration on pain breathing intervention may have induced a general loss of
perception. In detail, a control group was missing, which somatosensory perception. In support of our observation,
had to breathe at similar respiration depths and rates, a multitude of studies report significant decreases in
however without the possibility of relaxation. For this late somatosensory event-related potentials (SERP) in
reason, our study suggests relaxation as an essential pre- response to nociceptive stimulation during hypnotic anal-
requisite of a DSB technique in efficiently modulating pain gesia [73,74]. De Pascalis et al. found increases in
perception. sensory and pain thresholds mirrored by a reduction of
certain components of the cortical SERP across different
A nonspecific psychomotor effect following the DSB inter- hypnosis conditions [75]. In this context, it is tempting to
vention may have been associated with relaxation, thus speculate that relaxation may exert its effect on soma-
providing a nonspecific increase in detection and pain tosensory perception by inhibiting thalamocortical activity
thresholds, as fatigue and a reduction in alertness both via a frontal cortex feedback loop [73].
were found to slightly increase mean reaction times [69].
However, in our study, fatigue was equivalent in both Moreover, our study revealed a significant decrease of
groups and did not change significantly during the DSB SCLs in all of the three microcycles indicating a slowing
interventions. In addition, it has been shown recently that down of sympathetic activity clearly restricted to the rDSB
mental fatigue did not affect the temporal preparation time condition. The changes of pain thresholds and SCLs were
in a choice reaction time task [70]. Moreover, such inversely correlated in the rDSB condition.
changes, if any, are unlikely to explain a threshold differ-
ence of approximately 1°C in our study, as this would As the changes of SCL and detection and pain thres-
afford reduced reaction times of almost 1 second. Inter- holds were only weakly correlated, we would strongly
estingly, following two yoga-based relaxation techniques, suggest discussing any potential (causal or not causal)
221
Busch et al.
0,20
Microcycle 1 Microcycle 4 Microcycle 6 overall
aDSB
Skin conductance levels
0,10
rDSB
0,00
Δ Change (%)
p=ns(.41)
-0,10
-0,20
-0,30
***
-0,50
0,20
Gain of function
0,00
Loss of function
Detection thresholds
-0,20
p=ns(.20)
z-transformed
-0,40
Δ Change
-0,60
-0,80
-1,00
-1,20
***
-1,40 p<.001
0,20
0,10
Gain of function
0,00
p=ns(.62)
Pain thresholds
z-transformed
Loss of function
-0,10
Δ Change
-0,20
-0,30
-0,40
***
p<.001
-0,50
-0,60
Figure 2 Mean changes of skin conductance level and detection and pain thresholds. Mean changes
(⫾standard deviation) and post hoc analyses of skin conductance levels and of the z-transformed detection
and pain thresholds from the first, fourth, and sixth microcycles and overall for both breathing interventions.
aDSB = attentive deep and slow breathing; rDSB = relaxing deep and slow breathing; ***P < 0.001;
ns = nonsignificant.
222
Effect of Breathing on Pain Perception
Nonparametric comparisons (Wilcoxon tests) of the profile of mood states and the total mood disturbances before (pre) and after (post) the aDSB and rDSB intervention. Values are
(0.83)
(0.68)
(0.33)
(0.83)
(0.17)
(0.51)
(0.55)
aDSB = attentive deep and slow breathing; rDSB = relaxing deep and slow breathing; M = mean; SD = standard deviation; Z = test statistic; P = significance; ns = nonsignificant.
ment with other studies investigating the effects of deep
aDSB vs rDSB
Comparison relaxation techniques on the autonomic nerve system. As
ns
ns
ns
ns
ns
ns
ns
P
has already been demonstrated, the basal electrodermal
activity was significantly reduced during meditation [76],
-0.21
-0.41
-0.98
-0.22
-1.36
-0.66
-0.59
mindfulness-based stress reduction [77], or an integrative
Z body–mind training [78]. In contrast, the aDSB mode
along with a concentration task did not reduce, but rather
ns (0.53)
ns (0.19)
ns (0.06)
<0.001 tended to increase the sympathetic arousal in our sample.
<0.01 As a potential mechanism underlying this phenomenon,
<0.01
<0.01
the attentional demands during the aDSB may have main-
P
<0.05
6.62
5.42
3.62
16.42
6.24
4.71
9.87
Confusion
Tension
Fatigue
223
Busch et al.
processing in patients with chronic back pain [93] or major ings. However, we are aware that a potential decrease in
depression [94], indicating that affective and sensory pain experimental pain perception due to DSB interventions in
processing may follow different courses. Interestingly, pain patients does not inevitably mean a significant alle-
DSB without a relaxation component was shown to be viation of their clinical pain. Further studies should be
ineffective in reducing pain levels, although most of the provided focusing on the effects of DSB techniques on
subjects felt it was useful and increased the patient’s patients with different pain syndromes and including
feeling of rapport [95]. Therefore, different factors apart different pain modalities.
from relaxation may drive mood improvement in breathing
techniques. One possible explanation may be based on Conclusions
psychological reasons, grounded in the subject’s expec-
tation, that a breathing intervention, commonly known as Taken together, our results suggest that the way of breath-
an effective stress reduction strategy, is able to attenuate ing decisively influences autonomic and pain processing.
224
Effect of Breathing on Pain Perception
plaints, anxiety and breathing pattern in patients 18 Zautra AJ, Fasman R, Davis MC, Craig AD. The effects
with hyperventilation syndrome and anxiety disorders. of slow breathing on affective responses to pain
J Psychosom Res 1996;41:481–93. stimuli: An experimental study. Pain 2010;149:12–8.
5 Jerath R, Edry JW, Barnes VA, Jerath V. Physiology of 19 McDonnell L, Bowden ML. Breathing management:
long pranayamic breathing: Neural respiratory ele- A simple stress and pain reduction strategy for use
ments may provide a mechanism that explains how on a pediatric service. Issues Compr Pediatr Nurs
slow deep breathing shifts the autonomic nervous 1989;12:339–44.
system. Med Hypotheses 2006;67:566–71.
20 Arch JJ, Craske MG. Mechanisms of mindfulness:
6 Mourya M, Mahajan AS, Singh NP, Jain AK. Effect of Emotion regulation following a focused breathing
slow- and fast-breathing exercises on autonomic func- induction. Behav Res Ther 2006;44:1849–58.
225
Busch et al.
33 Marx R, Scheibenbogen O. Visualisierung der Respi- 46 Wallenstein S, Fisher AC. The analysis of the two-
ration als verhaltenstherapeutische Intervention period repeated measurements crossover design
bei Angsterkrankungen. Foto-Medico—Internationaler with application to clinical trials. Biometrics 1977;33:
Arbeitskreis für Medizinische Bilddokumentation 261–9.
1999;9:7–9.
47 Venables PH, Martin I. The relation of palmar sweat
34 Brown RP, Gerbarg PL. Yoga breathing, meditation, gland activity to level of skin potential and conduc-
and longevity. Ann N Y Acad Sci 2009;1172:54–62. tance. Psychophysiology 1967;3:302–11.
35 Paul G, Elam B, Verhulst SJ. A longitudinal study 48 Fuhrer MJ. Stimulus site effects on skin conductance
of students’ perceptions of using deep breathing responses from the volar surfaces. Psychophysiology
1974;11:365–71.
39 Ehrmann W. Handbuch der Atemtherapie. Ahlerstedt: 53 McNair PM, Lorr M, Droppleman LF. POMS Manual:
Param-Verlag; 2004. Profile of Mood States. San Diego, CA: Educational
and Industrial Testing Service; 1992.
40 Wang SZ, Li S, Xu XY, et al. Effect of slow abdominal
breathing combined with biofeedback on blood pres- 54 McNair D, Lorr M, Droppleman L. Profile of Mood
sure and heart rate variability in prehypertension. States POMS—Ein Verfahren zur Messung von Stim-
J Altern Complement Med 2010;16:1039–45. mungszuständen. In: CIPS, ed. Internationale Skalen
für Psychiatrie. Weinheim: Beltz Test Gesellschaft;
41 Minyaev V, Petushkov M. Voluntary control of thoracic 1981:1–5.
and abdominal respiratory movements. Hum Physiol
2005;31:44–8. 55 Lira FT, Fagan TJ. The profile of mood states: Norma-
tive data on a delinquent population. Psychol Rep
1978;42:640–2.
42 Fruhstorfer H, Lindblom U, Schmidt WC. Method for
quantitative estimation of thermal thresholds in
56 Pollock V, Cho DW, Reker D, Volavka J. Profile of
patients. J Neurol Neurosurg Psychiatry 1976;39:
Mood States: The factors and their physiological cor-
1071–5.
relates. J Nerv Ment Dis 1979;167:612–4.
43 Rolke R, Baron R, Maier C, et al. Quantitative sensory 57 Cui J, Matsushima E, Aso K, Masuda A, Makita K.
testing in the German Research Network on Neuro- Psychological features and coping styles in patients
pathic Pain (DFNS): Standardized protocol and refer- with chronic pain. Psychiatry Clin Neurosci 2009;63:
ence values. Pain 2006;123:231–43. 147–52.
44 Magerl W, Krumova EK, Baron R, et al. Reference 58 Jungquist CR, O’Brien C, Matteson-Rusby S, et al.
data for quantitative sensory testing (QST): Refined The efficacy of cognitive-behavioral therapy for insom-
stratification for age and a novel method for statistical nia in patients with chronic pain. Sleep Med 2010;11:
comparison of group data. Pain 2010;151:598–605. 302–9.
45 Glass GV, Stanley JC. Statistical Methods in Educa- 59 Malouff JM, Schutte NS, Ramerth W. Evaluation of a
tion and Psychology. Boston, MA: Allyn & Bacon; short form of the POMS-Depression scale. J Clin
1970. Psychol 1985;41:389–91.
226
Effect of Breathing on Pain Perception
60 Casten RJ, Parmelee PA, Kleban MH, Lawton MP, changes to noxious stimuli and 2. Transfer learning to
Katz IR. The relationships among anxiety, depression, reduce chronic low back pain. Int J Clin Exp Hypn
and pain in a geriatric institutionalized sample. Pain 1998;46:92–132.
1995;61:271–6.
74 Zachariae R, Bjerring P. Laser-induced pain-related
61 Knight WE, Rickard Ph DN. Relaxing music prevents brain potentials and sensory pain ratings in high and
stress-induced increases in subjective anxiety, systolic low hypnotizable subjects during hypnotic sugges-
blood pressure, and heart rate in healthy males and tions of relaxation, dissociated imagery, focused anal-
females. J Music Ther 2001;38:254–72. gesia, and placebo. Int J Clin Exp Hypn 1994;42:
56–80.
62 Iwanaga M, Moroki Y. Subjective and physiological
64 Lyvers M, Miyata Y. Effects of cigarette smoking on 76 Travis F. Autonomic and EEG patterns distinguish
electrodermal orienting reflexes to stimulus change transcending from other experiences during Trans-
and stimulus significance. Psychophysiology 1993;30: cendental Meditation practice. Int J Psychophysiol
231–6. 2001;42:1–9.
65 Zahn TP, Rapoport JL. Autonomic nervous system 77 Lush E, Salmon P, Floyd A, et al. Mindfulness medi-
effects of acute doses of caffeine in caffeine users and tation for symptom reduction in fibromyalgia: Psycho-
abstainers. Int J Psychophysiol 1987;5:33–41. physiological correlates. J Clin Psychol Med Settings
2009;16:200–7.
66 Cohen J. Statistical Power Analysis for the Behavioral
Sciences. Hillsdale, NJ: Lawrence Earlbaum Associ- 78 Tang YY, Ma Y, Fan Y, et al. Central and autonomic
ates; 1988. nervous system interaction is altered by short-term
meditation. Proc Natl Acad Sci U S A 2009;106:8865–
67 Morris SB, DeShon RP. Combining effect size esti- 70.
mates in meta-analysis with repeated measures
and independent-groups designs. Psychol Methods 79 Holmes DS, McCaul KD, Solomon S. Control of res-
2002;7:105–25. piration as a means of controlling responses to threat.
J Pers Soc Psychol 1978;36:198–204.
68 Grant JA, Rainville P. Pain sensitivity and analgesic
effects of mindful states in Zen meditators: A cross- 80 Clark ME, Hirschman R. Effects of paced respiration
sectional study. Psychosom Med 2009;71:106–14. on anxiety reduction in a clinical population. Biofeed-
back Self Regul 1990;15:273–84.
69 Appelle S, Oswald LE. Simple reaction time as a func-
tion of alertness and prior mental activity. Percept Mot 81 Victor RG, Leimbach WN Jr, Seals DR, Wallin BG,
Skills 1974;38:1263–8. Mark AL. Effects of the cold pressor test on muscle
sympathetic nerve activity in humans. Hypertension
70 Langner R, Steinborn MB, Chatterjee A, Sturm W, 1987;9:429–36.
Willmes K. Mental fatigue and temporal preparation
in simple reaction-time performance. Acta Psychol 82 Martinez-Lavin M, Hermosillo AG. Autonomic nervous
(Amst) 2010;133:64–72. system dysfunction may explain the multisystem
features of fibromyalgia. Semin Arthritis Rheum
71 Subramanya P, Telles S. Performance on psycho- 2000;29:197–9.
motor tasks following two yoga-based relaxation
techniques. Percept Mot Skills 2009;109:563–76. 83 Qiao ZG, Vaeroy H, Morkrid L. Electrodermal and
microcirculatory activity in patients with fibromyalgia
72 Kaul P, Passafiume J, Sargent CR, O’Hara BF. Medi- during baseline, acoustic stimulation and cold pressor
tation acutely improves psychomotor vigilance, and tests. J Rheumatol 1991;18:1383–9.
may decrease sleep need. Behav Brain Funct
2010;6:1–9. 84 Cohen H, Neumann L, Shore M, et al. Autonomic
dysfunction in patients with fibromyalgia: Application
73 Crawford HJ, Knebel T, Kaplan L, et al. Hypnotic of power spectral analysis of heart rate variability.
analgesia: 1. Somatosensory event-related potential Semin Arthritis Rheum 2000;29:217–27.
227
Busch et al.
85 Ozgocmen S, Ozyurt H, Sogut S, Akyol O. Current 92 Kubzansky LD, Wright RJ, Cohen S, et al. Breathing
concepts in the pathophysiology of fibromyalgia: easy: A prospective study of optimism and pulmonary
The potential role of oxidative stress and nitric oxide. function in the normative aging study. Ann Behav Med
Rheumatol Int 2006;26:585–97. 2002;24:345–53.
86 Hassett AL, Radvanski DC, Vaschillo EG, et al. A pilot 93 Dickens C, Jayson M, Sutton C, Creed F. The rela-
study of the efficacy of heart rate variability (HRV) tionship between pain and depression in a trial using
biofeedback in patients with fibromyalgia. Appl Psy- paroxetine in sufferers of chronic low back pain. Psy-
chophysiol Biofeedback 2007;32:1–10. chosomatics 2000;41:490–9.
87 Craig AD. A new view of pain as a homeostatic 94 Kundermann B, Hemmeter-Spernal J, Huber MT,
emotion. Trends Neurosci 2003;26:303–7. Krieg JC, Lautenbacher S. Effects of total sleep dep-
89 Kim KS, Lee SW, Choe MA, et al. Effects of abdominal 95 Downey LV, Zun LS. The effects of deep breath-
breathing training using biofeedback on stress, ing training on pain management in the emer-
immune response and quality of life in patients with a gency department. South Med J 2009;102:
mastectomy for breast cancer. Taehan Kanho Hakhoe 688–92.
Chi 2005;35:1295–303.
96 Fulwiler CE, Saper CB. Subnuclear organization of the
90 Tweeddale PM, Rowbottom I, McHardy GJ. Breathing efferent connections of the parabrachial nucleus in the
retraining: Effect on anxiety and depression scores in rat. Brain Res 1984;319:229–59.
behavioural breathlessness. J Psychosom Res
1994;38:11–21. 97 Yasui Y, Tsumori T, Oka T, Yokota S. Amygdaloid
axon terminals are in contact with trigeminal premotor
91 Gaines T, Barry LM. The effect of a self-monitored neurons in the parvicellular reticular formation of
relaxation breathing exercise on male adolescent the rat medulla oblongata. Brain Res 2004;1016:129–
aggressive behavior. Adolescence 2008;43:291–302. 34.
228