Stimulation by central command of locomotion, respiration and circulation during exercise

doi:10.1016/0034-5687(85)90136-7

Respiration Physiology

Volume 59, Issue 3, March 1985, Pages 313-337

Respiration Physiolo...

https://doi.org/10.1016/0034-5687(85)90136-7 Get rights and content

Abstract

We studied the relationships between exercise (locomotion) and respiratory and circulatory responses in 19 cats that walked or ran normally on a treadmill, and in 16 paralyzed animals during fictive locomotion, i.e., locomotory activity in motor nerves to the legs. Preparation included anesthetized cats with intact brains and unanesthetized decorticate (hypothalamic) and decerebrate (mesencephalic) animals. Spontaneous actual locomotion and fictive locomotion occurred in al preparations except the mesencephalic cats. Electrical stimulation or injection of a GABA antagonist (picrotoxin) into the hypothalamic locomotor region caused locomotion to develop. In all cases when locomotion occurred, respiration and arterial pressure increased in proportion to the level of locomotor activity despite control or ablation of respiratory feedback mechanisms. Respiration and arterial pressure increased similarly during fictive locomotion despite the absence of muscular contraction or limb movement and the lack of change of metabolic rate. We conclude that the study provides experimental support for the feed-forward, or command signal, hypothesis for the genesis of proportional changes of respiration and circulation that occur during exercise. Feedback mechanisms are not required for its operation. We suggest that command signals emanting from the hypothalamus provide the primary drive for changes of respiration and circulation during exercise.

References (51)

J. Duffin et al.
The ventilatory response to carbon dioxide in hyperoxic exercise
Respir. Physiol.
(1980)
F.L. Eldridge et al.
Central neural respiratory drive and afterdischarge
Respir. Physiol.
(1980)
R. Flandrois et al.
Control of breathing in the exercising dog
Respir. Physiol.
(1971)
W.E. Fordyce et al.
Evidence in man for a fast neural mechanism during the early phase of exercise hyperpnea
Respir. Physiol.
(1982)
J.G. Henry et al.
Human core temperature increase as a stimulus to breathing during moderate exercise
Respir. Physiol.
(1974)
C.L. Jasinskas et al.
Entrainment of breathing rate to movement frequency during work at two intensities
Respir. Physiol.
(1980)
L.M. Jordan et al.
Locomotin evoked by brainsteim stimulation occurence without phasic segmental afferent input
Brain Res.
(1979)
M.A. Kelley et al.
Hypercapnic ventilation during exercise: Effect of exercise methods and inhalation techniques
Respir. Physiol.
(1982)
C.A. Smith et al.
Ventilatory response of goats to treadmill exercise: Grade effects
Respir. Physiol.
(1983)
B.J. Whipp et al.
Effect of body temperature on the ventilatory response to exercise
Respir. Physiol.
(1970)

E. Asmussen et al.

On the nervous factors controlling respiration and circulation during exercise. Experiments with curarization

Acta Physiol. Scand.

(1965)

R. Casaburi et al.

Ventilatory and gas exchange dynamics in response to sinusoidal work

J. Appl. Physiol.

(1977)

B.A. Cross et al.

The pH oscillation in arterial blood during exercise: a potential signal for the ventilatory response in the dog

J. Physiol. (London)

(1982)

P. Dejours

Control of respiration in muscular exercise

A.F. DiMarco et al.

Immmediate changes in ventilation and respiratory pattern with onset and cessation of locomotion in the cat

J. Physiol. (London)

(1983)

F.L. Eldridge

Relationship between phrenic nerve activity and ventilation

Am. J. Physiol.

(1971)

F.L. Eldridge

Central neural respiratory stimulatory effect of active respiration

J. Appl. Physiol.

(1974)

F.L. Eldridge

Relationship between respiratory nerve and muscle activity and muscle force output

J. Appl. Physiol.

(1975)

F.L. Eldridge et al.

Exercise hyperpnea and locomotion: Parallel activation from the hypothalamus

Science

(1981)

H.V. Forster et al.

Hyperpnea of exercise at various Pi_O₂ in normal and carotid body-denervated ponies

J. Appl. Physiol.

(1983)

R.F. Fregosi et al.

Arterial blood acid-base regulation during exercise in rats

J. Appl. Physiol.

(1984)

E. Garcia-Rill et al.

Chemical activation of the mesencephalic lomotor region

Soc. Neurosci. Abstr.

(1983)

G.M. Goodwin et al.

Cardiovascular and respiratory responses to changes in central command during isometric exercise at constant muscle tension

J. Physiol. (London)

(1972)

J.F. Green et al.

Ventilatory changes associated with changes in pulmonary blood flow in dogs

J. Appl. Physiol.

(1983)

A.B. Hastings et al.

Comparative physiological responses to exercise stress

J. Appl. Physiol.

(1982)

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The cardiovascular response is appropriately regulated during exercise to meet the metabolic demands of the active muscles. The exercise pressor reflex is a neural feedback mechanism through thin-fiber muscle afferents activated by mechanical and metabolic stimuli in the active skeletal muscles. The mechanical component of this reflex is referred to as skeletal muscle mechanoreflex. Its initial step requires mechanotransduction mediated by mechanosensors, which convert mechanical stimuli into biological signals. Recently, various mechanosensors have been identified, and their contributions to muscle mechanoreflex have been actively investigated. Nevertheless, the mechanosensitive channels responsible for this muscular reflex remain largely unknown. This review discusses progress in our understanding of muscle mechanoreflex under healthy conditions, focusing on mechanosensitive channels.
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We compared cardiopulmonary responses to arm-ergometry in individuals with cervical spinal cord injury (C-SCI) and able-bodied controls. We hypothesized that individuals with C-SCI would have higher respiratory frequency (f_b) but lower tidal volume (VT) at a given work rate and dynamically hyperinflate during exercise, whereas able-bodied individuals would not. Participants completed pulmonary function testing, an arm-ergometry test to exhaustion, and a sub-maximal exercise test consisting of four-minute stages at 20, 40, 60, and 80% peak work rate. Able-bodied individuals completed a further sub-maximal test with absolute work rate matched to C-SCI. During work rate matched sub-maximal exercise, C-SCI had smaller VT (main effect p < 0.001) compensated by an increased f_b (main effect p = 0.009). C-SCI had increased end-expiratory lung volume at 80% peak work rate vs. rest (p < 0.003), whereas able-bodied did not. In conclusion, during arm-ergometry, individuals with C-SCI exhibit altered ventilatory patterns characterized by reduced VT, higher f_b, and dynamic hyperinflation that may contribute to the observed reduced aerobic exercise capacity.
Effects of acute hyperglycemia on the exercise pressor reflex in healthy rats
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The exercise pressor reflex is exaggerated in type 2 diabetes mellitus (T2DM). Hyperglycemia, a main characteristic of T2DM, likely contributes to this exaggerated response. However, the isolated effect of acute hyperglycemia, independent of T2DM, on the exercise pressor reflex is not known. Therefore, the purpose of this study was to determine the effect of acute, local exposure to hyperglycemia on the exercise pressor reflex and its two components, namely the mechanoreflex and the metaboreflex, in healthy rats. To accomplish this, we determined the effect of an acute locol intra-arterial glucose infusion (0.25 g/mL) on cardiovascular responses to static contraction (i.e., exercise pressor reflex) and tendon stretch (i.e., mechanoreflex) for 30 s, as well as hindlimb intra-arterial lactic acid (24 mM) injection (i.e., metaboreflex) in fasted unanesthetized, decerebrated Sprague-Dawley rats. We measured and compared changes in mean arterial pressure (MAP) and heart rate (HR) before and after glucose infusion. We found that acute glucose infusion did not affect the pressor response to static contraction (ΔMAP: before: 15 ± 2 mmHg, after: 12 ± 2 mmHg; n = 8, p > 0.05), tendon stretch (ΔMAP: before: 12 ± 1 mmHg, after: 12 ± 3 mmHg; n = 8, p > 0.05), or lactic acid injection (ΔMAP: before: 13 ± 2 mmHg, after: 17 ± 3 mmHg; n = 9, p > 0.05). Likewise, cardioaccelerator responses were unaffected by glucose infusion, p > 0.05 for all. In conclusion, these findings suggest that acute, local exposure to hyperglycemia does not affect the exercise pressor reflex or either of its components.
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Citation Excerpt :
Mechanisms primarily responsible for these autonomic alterations include central command, the exercise pressor reflex, and arterial baroreflexes. Central command, a feed-forward mechanism arising from higher brain centers evokes parallel activation of locomotor activity and autonomic outflow (Eldridge et al., 1985; Goodwin et al., 1972), and is, in turn, thought to be significantly influenced by the “effort sense” of the activity (Williamson et al., 2001, 2006). The exercise pressor reflex, a feed-back mechanism arising from the contracting muscle, reflexively adjusts sympathetic outflow (Alam and Smirk, 1938; McCloskey and Mitchell, 1972) and is, in turn, greatly influenced by the metabolic milieu in the exercising muscle (Adreani and Kaufman, 1998; Kaufman et al., 1984; Rotto and Kaufman, 1988).
Autonomic alterations at the onset of exercise are critical to redistribute cardiac output towards the contracting muscles while preventing a fall in arterial pressure due to excessive vasodilation within the contracting muscles. Neural mechanisms responsible for these adjustments include central command, the exercise pressor reflex, and arterial and cardiopulmonary baroreflexes. The exercise pressor reflex evokes reflex increases in sympathetic activity to the heart and systemic vessels and decreases in parasympathetic activity to the heart, which increases blood pressure (BP), heart rate, and total peripheral resistance through vasoconstriction of systemic vessels. In this review, we discuss recent advancements in our understanding of exercise pressor reflex function in health and disease. Specifically, we discuss emerging evidence suggesting that sympathetic vasoconstrictor drive to the contracting and non-contracting skeletal muscle is differentially controlled by central command and the metaboreflex in healthy conditions. Further, we discuss evidence from animal and human studies showing that cardiovascular diseases, including hypertension, diabetes, and heart failure, lead to an altered exercise pressor reflex function. We also provide an update on the mechanisms thought to underlie this altered exercise pressor reflex function in each of these diseases. Although these mechanisms are complex, multifactorial, and dependent on the etiology of the disease, there is a clear consensus that several mechanisms are involved. Ultimately, approaches targeting these mechanisms are clinically significant as they provide alternative therapeutic strategies to prevent adverse cardiovascular events while also reducing symptoms of exercise intolerance.
Exaggerated exercise pressor reflex in type 2 diabetes: Potential role of oxidative stress
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Type 2 diabetes mellitus (T2DM) leads to exaggerated cardiovascular responses to exercise, in part due to an exaggerated exercise pressor reflex. Accumulating data suggest excessive oxidative stress contributes to an exaggerated exercise pressor reflex in cardiovascular-related diseases. Excessive oxidative stress is also a primary underlying mechanism for the development and progression of T2DM. However, whether oxidative stress plays a role in mediating the exaggerated exercise pressor reflex in T2DM is not known. Therefore, this review explores the potential role of oxidative stress leading to increased activation of the afferent arm of the exercise pressor reflex. Several lines of evidence support direct and indirect effects of oxidative stress on the exercise pressor reflex. For example, intramuscular ROS may directly and indirectly (by attenuating contracting muscle blood flow) increase group III and IV afferent activity. Oxidative stress is a primary underlying mechanism for the development of neuropathic pain, which in turn is associated with increased group III and IV afferent activity. These are the same type of afferents that evoke muscle pain and the exercise pressor reflex. Furthermore, oxidative stress-induced release of inflammatory mediators may modulate afferent activity. Collectively, these alterations may result in a positive feedback loop that further amplifies the exercise pressor reflex. An exaggerated reflex increases the risk of adverse cardiovascular events. Thus, identifying the contribution of oxidative stress could provide a potential therapeutic target to reduce this risk in T2DM.
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Stimulation by central command of locomotion, respiration and circulation during exercise

Abstract

Respir. Physiol.

Respir. Physiol.

Respir. Physiol.

Respir. Physiol.

Respir. Physiol.

Respir. Physiol.

Brain Res.

Respir. Physiol.

Respir. Physiol.

Respir. Physiol.

On the nervous factors controlling respiration and circulation during exercise. Experiments with curarization

Acta Physiol. Scand.

Ventilatory and gas exchange dynamics in response to sinusoidal work

J. Appl. Physiol.

The pH oscillation in arterial blood during exercise: a potential signal for the ventilatory response in the dog

J. Physiol. (London)

Control of respiration in muscular exercise

Immmediate changes in ventilation and respiratory pattern with onset and cessation of locomotion in the cat

J. Physiol. (London)

Relationship between phrenic nerve activity and ventilation

Am. J. Physiol.

Central neural respiratory stimulatory effect of active respiration

J. Appl. Physiol.

Relationship between respiratory nerve and muscle activity and muscle force output

J. Appl. Physiol.

Exercise hyperpnea and locomotion: Parallel activation from the hypothalamus

Science

Hyperpnea of exercise at various PiO2 in normal and carotid body-denervated ponies

J. Appl. Physiol.

Arterial blood acid-base regulation during exercise in rats

J. Appl. Physiol.

Chemical activation of the mesencephalic lomotor region

Soc. Neurosci. Abstr.

Cardiovascular and respiratory responses to changes in central command during isometric exercise at constant muscle tension

J. Physiol. (London)

Ventilatory changes associated with changes in pulmonary blood flow in dogs

J. Appl. Physiol.

Comparative physiological responses to exercise stress

J. Appl. Physiol.

Hyperpnea of exercise at various Pi_O₂ in normal and carotid body-denervated ponies