Relationship between carotid chemoreceptor activity and ventilation in the cat

doi:10.1016/0034-5687(75)90018-3

Respiration Physiology

Volume 24, Issue 3, September 1975, Pages 267-286

Respiration Physiolo...

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Abstract

The steady-state stimulus-response relations between arterial pq, and P_CO₂, and the mean activity of carotid chemoreceptors (single and multi-fiber) and ventilation were simultaneously recorded in 48 anesthetized cats. The carotid chemoreceptor activity varied linearly with the increase of arterial P_CO₂, below and above the normal value, at any given level of arterial P_O₂. A decrease in arterial Po, increased the activity of the carotid chemoreceptors and increased its sensitivity to changes in arterial P_CO₂ showing multiplicative stimulus interaction. The authors also found that the response in ventilation during hypoxia to changes in arterial P_CO₂, below the normal value was smaller than that to changes above it, unlike the response of carotid chemoreceptors. This arterial P_CO₂, quasi-threshold for ventilation was, therefore, not due to a corresponding threshold for the activity of the carotid chemoreceptors but to a central mechanism. Above the central Pa_CO₂ threshold, the ventilatory response to changes in Pa_CO₂, and Pa_O₂ resembled that of chemoreceptors but the ventilation dependent on hypoxia was greater than that could be directly accounted for by the activity of peripheral chemoreceptors. A multiplicative interaction between the activity of peripheral chemoreceptors and central CO₂ excitation appears to play a role in the regulation of ventilation.

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Citation Excerpt :
Unfortunately, isolating central and peripheral chemoreceptor compartments is challenging in humans. Unlike central chemoreceptors, peripheral chemoreceptors regulate ventilation quickly (10–15 s; Pedersen et al., 2004; Smith et al., 2006) through a synergistic polymodal response (e.g., hypercapnia and hypoxia; Lahiri and DeLaney, 1975; Daristotle et al., 1987; Duffin, 2005), while the central chemoreceptors are slower to respond (∼25–30 s; Smith et al., 2006). Under natural conditions, the faster response time of peripheral chemoreceptors may mask central chemoreceptor responses, making isolation and observation of CCRC activity in humans difficult (Smith et al., 2006).
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The peripheral and central chemoreceptors provide negative feedback control of respiratory motor output in response to fluctuating partial pressures of O2 and CO2. The interaction between CO2 and O2 at the level of the carotid body chemoreceptors is well-known (hypercapnia potentiates the hypoxic response (Lahiri and DeLaney, 1975)). How the peripheral (PCR) and central (CCR) chemoreflexes interact centrally to modify respiratory motor output is less clear, seemingly varying with species and/or experimental approach.
The potential for interaction between the peripheral (PCR) and central (CCR) chemoreflexes has not been studied in the neonatal period, when breathing is inherently unstable. Based on recent work in adult rodents, this study addresses the hypothesis that in neonatal mice there is a hypoadditive interaction between the chemoreflexes. To test this, a mask-pneumotach system was used to expose postnatal day (P) 11–12 mouse pups to square-wave hyperoxia (100% O₂; n = 8) or hypoxia (10% O₂; n = 11), administered in normocapnic conditions (inspired CO₂ (F_ICO₂) = 0.001–0.005), or following an episode of re-breathing to increase F_ICO₂ by 0.015–0.02. The immediate (i.e. PCR-mediated) responses of frequency (f_B), tidal volume (V_T) and ventilation ( ${\dot{V}}_{E}$ ) to square-wave hyperoxia and hypoxia were assessed. When given in a normocapnic background, hyperoxia induced an immediate (within the first 20 breaths, or ∼6 s) but transient fall in f_B (−46 ± 9 breaths/min) and ${\dot{V}}_{E}$ (−149 ± 41 μl min⁻¹ g⁻¹) (P < 0.001 for both), with no effect on V_T. In contrast, hyperoxia had no influence on breathing when it was administered following re-breathing. Similarly, the hypoxia-induced increase in f_B was greater when applied under normocapnic conditions (50 ± 8 breaths/min) then when applied following re-breathing (21 ± 5 breaths/min) (P = 0.02). These data demonstrate a hypo-additive interaction between the PCR and CCR with respect to the immediate frequency response to inhibition or excitation of the PCR. Hypoaddition of the chemoreflexes could cause or mitigate neonatal apnea, depending on the prevailing PCO₂.
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Central respiratory chemosensitivity is mediated via chemoreceptor neurons located throughout brain stem tissue. These receptors detect proximal CO₂/[H⁺] (i.e., controller gain) and modulate breathing in a classic negative feedback loop. Loop gain (responsiveness) is the theoretical product of controller (chemoreceptors), mixing/feedback (cardiovascular and cerebrovascular systems), and plant (pulmonary system) gains. The level of chemoreceptor stimulation is determined by interactions between mixing and plant gains. The extent to which steady-state changes in body position may affect central chemoreflex loop gain in response to CO₂ is unclear. Because of the potential effects of tilt on pulmonary mechanics, we hypothesized that plant gain would be altered by head-up and head-down tilt (HUT, HDT) during hyperoxic rebreathing, which theoretically isolates plant gain by eliminating systemic arterial–tissue gradients. Sixteen subjects (eight females) underwent hyperoxic rebreathing tests on a tilt table to quantify central chemoreflex loop gain in five steady-state positions: 90° HUT, 45° HUT, supine, 45° HDT, and 90° HDT. Respiratory responses (tidal volume, V_T; frequency, f_R; minute ventilation, V_E) were quantified during steady-state and increases in CO₂ during rebreathing by linear regression above the ventilatory recruitment threshold (VRT). Using one-factor analysis of variance, we found that there were no differences in the respiratory responses between the five positions (VRT, P = 0.711; V_T, P = 0.290; f_R, P = 0.748; V_E, P = 0.325). Our findings suggest that during steady-state orthostatic stress, the ability of subjects to mount a normal ventilatory response to increased CO₂ was unaffected, despite any potential changes in pulmonary mechanics associated with positional challenges.
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The potential differences in cerebrovascular responses between the anterior and posterior circulations to changes in CO₂ are unclear in humans. Using transcranial Doppler ultrasound, we compared the CO₂ reactivity of the (1) BA and PCA and (2) MCA and PCA during hyperoxic rebreathing in supine position. The reactivity in the BA and PCA was similar in both absolute (1.27 ± 0.5 and 1.27 ± 0.6 cm/s/Torr; P = 0.992) and relative (3.98 ± 1.3 and 3.66 ± 1.5%/Torr CO₂; P = 0.581) measures, suggesting that the PCA is an adequate surrogate measure of reactivity for the BA. The MCA reactivity was greater than the PCA in absolute (2.09 ± 0.7 and 1.22 ± 0.5 cm/s/Torr CO₂; P < 0.001), but not relative measures (3.25 ± 1.0 and 3.56 ± 1.6%/Torr CO₂; P = 0.629). Our findings (a) confirm regional differences in the absolute reactivity in the human brain and (b) suggest that in cerebrovascular studies investigating functions mediated by posterior brain structures (e.g., control of breathing), the posterior vasculature should also be insonated.
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^☆: Supported in part by USPHS Grant HL-08805.

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Relationship between carotid chemoreceptor activity and ventilation in the cat☆

Abstract

Respir. Physiol.

Respir. Physiol.

Respir. Physiol.

Respir. Physiol.

Respir. Physiol.

Respir. Physiol.

Respir. Physiol.

Respir. Physiol.

Respir. Physiol.

The relation between chemoreceptor discharge and respiratory fluctuation of arterial pH in the anesthetized cat

J. Physiol. (London)

The effect of hypoxia on the respiratory fluctuations in chemoreceptor discharge in the cat

J. Physiol. (London)

The frequency of nerve impulses in single carotid body chemoreceptor afferent fibers recorded in vivo with intact circulation

J. Physiol. (London)

The control system regulating breathing in man

Q. Rev. Biophys.

The importance of timing on the respiratory effects of intermittent carotid body chemoreceptor stimulation

J. Physiol. (London)

Chemoreceptor activity of the carotid body of the cat

J. Physiol. (London)

Statistical analysis of cyclic variations in carotid body chemoreceptor activity

J. Appl. Physiol.