Response of intrapulmonary chemoreceptors in the duck to changes in PCO2 and pH

doi:10.1016/0034-5687(78)90042-7

Respiration Physiology

Volume 35, Issue 1, October 1978, Pages 65-77

Respiration Physiolo...

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Abstract

We have estimated the relative importance of changes in blood P_CO₂ and pH in determining activity of intrapulmonary chemoreceptors (IPC) in the unidirectionally ventilated duck. The response of single unit vagal afferents from IPC to changing lung gas P_CO₂ was tested before and after changing blood pH by intravenous infusion of NaHCO₃. Using multiple linear regression analysis, we calculated how much of the change in IPC activity for a given change in P_CO₂ was due to the changing P_CO₂ at constant pH (CO₂ sensitivity) or to the change in pH concomitant with the change in P_CO₂ (H⁺ sensitivity). For 10 IPC, the CO₂ sensitivity was on the average 2.3 times larger than the H⁺ sensitivity. Changes in pH as well as P_CO₂ of lung blood should be considered in assessing the role of IPC in control of breathing.

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Microelectrode measurement of the intracellular pH and buffering power of mouse soleus muscle fibres
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Physiological parameters which determine P_CO₂ at the intrapulmonary chemoreceptor site in Gallus domesticus

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Cited by (13)

CO<inf>2</inf> transduction mechanisms in avian intrapulmonary chemoreceptors: Experiments and models
2004, Respiratory Physiology and Neurobiology
Intrapulmonary chemoreceptors (IPC) are neurons that sense tonic and phasic CO₂ stimuli in the lungs of birds and diapsid reptiles. IPC are different from most other vertebrate respiratory CO₂ receptors because: (1) they are stimulated by low $P_{C O_{2}}$ and inhibited by high $P_{C O_{2}}$ , (2) they have extremely rapid response characteristics, (3) their CO₂ sensitivity is nearly abolished by intracellular inhibitors of carbonic anhydrase, and (4) their CO₂ sensitivity is strongly depressed by inhibiting Na⁺/H⁺ antiport exchange. Experimental evidence suggests that IPC respond to intracellular pH, not CO₂ directly, and that intracellular pH and IPC discharge are determined by a kinetic balance between CO₂ hydration/dehydration rates, transmembrane acid/base exchange rates, and intracellular buffering. We review experimental evidence for and against various mechanisms of IPC CO₂ chemotransduction, present a conceptual and mathematical model of the proposed mechanisms, and compare this model to CO₂ transduction in other respiratory chemoreceptors.
Sodium bicarbonate infusion increases discharge frequency of intrapulmonary chemoreceptors only at high CO<inf>2</inf>
1986, Respiration Physiology
We felt that earlier determinations of independent effects of extracellular pH and P_CO₂ on intrapulmonary chemoreceptors (IPC) discharge frequency were difficult to analyze because they used perfused lungs, and ventilation-perfusion changes among parabronchi could not be controlled. We decided to repeat these studies in non-perfused lungs. We cannulated both extrapulmonary bronchi of 10 thoracotomized Pekin ducks anesthetized with sodium pentobarbital (25–35 mg/kg) and unidirectionally ventilated each lung. The perfused right lung mainteained gas exchange while the non-perfused left lung recieved 0.6 L/min of CO₂ mixed in air. We recorded the discharge frequency of one IPC per duck at various P_CO₂, re-established circulation, and infused 3.0 mmol/kg of sodium bicarbonate intravenously. After 15 min, discharge frequencies were again measured from the same IPC in the nonperfused lung. The slopes and intercepts of discharge frequencies vs ln P_CO₂ relationship were depressed in six IPC, increased in two IPC and not significantly affected in two IPC. Arterial pH was increased significantly (0.11 unit) at 38 Torr arterial P_CO₂. We conclude that acutely increased extracellular sodium bicarbonate affects IPC discharge only by depressing sensitivity of most IPC to P_CO₂ and does not have an independent effect through pH.
Ventilatory and intrapulmonary chemoreceptor sensitivity to CO<inf>2</inf> in the burrowing owl
1985, Respiration Physiology
We measured the ventilatory response of anesthetized, unidirectionally ventilated pigeons and burrowing owls to changes in intrapulmonary CO₂ concentration and the static CO₂ sensitivity of intrapulmonary chemoreceptors (IPC) in these species and the domestic goose. Compared with pigeons, burrowing owls showed a significantly reduced respiratory frequency and amplitude response to increases in FI_CO₂ from 0.05 to 0.10, which corroborates similar findings in intact, awake individuals of the same species.
The average static CO₂ sensitivity of IPC in geese, pigeons, and burrowing owls, as reflected by the average slope of the linear regressions of receptor discharge frequency ofn lnOI_CO₂, was −7.96, −11.1 and −6.87 imp/sec·ln(PI_CO₂), respectively. The sensitivities of individual receptros were normally distributed in geese and pigeons, but skewed in burrowing owls. Therefore, the median CO₂ sensitivity [−5.50 imp/sec·ln(PI_CO₂)] is a more appropriate measure of the typical CO₂ sensitivity of IPC in burrowing owls. The static CO₂ sensitivity of IPC in burrowing owls is the lowest reported for euthermic birds with a normal acid-base balance and may materially contribute to the blunted ventilatory response of these birds to the elevated CO₂ levels thery encounter in nature.
Acid-base balance during lactic acid infusion in the lizard varanus salvator
1985, Respiration Physiology
Although reptiles rely heavily on anaerobic metabolism and lactic acid production during activity, little is known concerning their ventilatory response to the attendant metabolic acidosis. We measured arterial P_CO₂, H⁺ and lactate (L) ion concentrations, and the rates of CO₂ (Ṁ_CO₂) and O₂ (Ṁ_O₂) exchange in Varanus salvator (n = 9) during intravenous infusions of lactic acid (HL) or sodium lactate (NaL; 250 mM) at rest. Two protocols were used: (1) 15 min infusions of 0.42 ml/min at both 25 and 35°C with measurements every 5 min; (2) 4.5 min infusions of 1.73 ml/min at 35°C with measurements at 4.5 min. At 35°C, control pH decreased from its value at 25°C with a slope of −0.007/°C and Pa_CO₂ increased. The results of HL infusion were: (1) [L]a increased, (2) Ṁ_CO₂ increased, (3) R (Ṁ_CO₂/Ṁ_O₂) increased, (4) pHa decreased, and (5) Pa_CO₂ remained unchanged from control ast both temperatures and at both infusion rates. The only significant changes in Pa_CO₂ observed were following the termination of fast HL infusions, when Pa_CO₂ decreased. In NaL infusions, only small changes were obeserved except in [L]a.
The results indicate that: (1) ΔpH/ΔT in V. salvator is less than in other poikilothermic vertebrates, but consistent with other varanid lizards, (2) respiratory compensation is slight in response to acute metabolic acidosis in this species, and (3) ventilation follows changes in Ṁ_CO₂ rather closely, accounting for precise regulation of Pa_CO₂ despite 4-fold increases in Ṁ_CO₂ elicited by bicarbonate buffering and increased metabolic rate.
Exercise hyperpnea in the duck without intrapulmonary chemoreceptor involvement
1983, Respiration Physiology
To determine the involvement of intrapulmonary chemoreceptors (IPC) in the control of breathing during exercise, it is necessary to hold the P_CO₂ in the microenvironment of these receptors constant at the resting value. We accomplished this in unanesthetized Pekin ducks by ligating the left pulmonary artery and diverting all of the cardiac output to the right lung, which was denervated. The ducks were then unidirectionally ventilated with a constant gas stream (5% CO₂, 19% O₂, balance N₂) at a flow rate of 12 L · min⁻¹. This procedure provided a constant microenvironment for the receptors in the left lung despite any changes in the chemical composition or flow rate of the blood going to the right lung during exercise.
Ventilatory effort increased during running exercise (1.44 km · h⁻¹ at a 3° incline) by an average of 145% over resting values because of an increase in both respiratory frequency and tidal volume. Because no altered stimuli were presented to the IPC using this procedure, the increased ventilation with exercise could not have resulted from changes in their discharge frequency.
We conclude that ventilation can increase during exercise in the duck in the absence of IPC involvement and that other neural input, possibly from muscle, is responsible for the hyperpnea.
The influence of alkalosis on panting
1980, Comparative Biochemistry and Physiology -- Part A: Physiology
- 1.
  1. The roles of pHa and Pa_co₂ in controlling respiration in unanesthetized chickens were studied during exposure to 45°C.
- 2.
  2. Control birds developed a profound respiratory alkalosis and had average respiratory frequencies of about 240 breaths/min.
- 3.
  3. Birds whose pHa was held constant by infusion of HCl showed maximal frequencies of less than 200 breaths/min while those with constant Pa_co₂ kept so by CO₂ inhalation, breathed slowest, at only 150 breaths/min.
- 4.
  4. We conclude that the alkalosis which develops in acute hyperthermia in the chicken is responsible for part of the increase in respiratory frequency to levels seen in panting.

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^∗: Present address: Department00 of Avian Science, University of California, Davis, CA 95616, U.S.A.

^∗∗: F. L. Powell was supported by a grant from the Deutscher Akademischer Austauschdienst (DAAD).

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Respiration Physiology

Abstract

References (24)

Intrapulmonary chemoreceptors in Gallus domesticus: adequate stimulus and functional localization

Respir. Physiol.

Blood as a physiochemical system XI. Man at rest

J. Biol. Chem.

Intrapulmonary CO₂ receptors in the duck: I. Stimulus specificity

Respir. Physiol.

Intracellular pH of isolated rat diaphragm muscle with metabolic and respiratory changes of extracellular pH

Respir. Physiol.

Classification of vagal afferents firing in phase with breathing in Gallus domesticus

Respir. Physiol.

Effects of CO₂ on pulmonary air flow resistance in the duck

Respir. Physiol.

Intrapulmonary chemoreceptors in Gallus domesticus

Respir. Physiol.

Ventilatory responses to CO₂ in the chicken: Intrapulmonary and systemic chemoreceptors

Respir. Physiol.

Intrapulmonary receptors in the Tegu lizard. II. Functional characteristics and localization

Respir. Physiol.

Microelectrode measurement of the intracellular pH and buffering power of mouse soleus muscle fibres

J. Physiol. (London)

Physiological parameters which determine P_CO₂ at the intrapulmonary chemoreceptor site in Gallus domesticus

The relationship between intracellular pH and potassium concentration in fromg brain in vivo

Bull. Europ. Physiopathol. Resp.

Cited by (13)

CO<inf>2</inf> transduction mechanisms in avian intrapulmonary chemoreceptors: Experiments and models

Sodium bicarbonate infusion increases discharge frequency of intrapulmonary chemoreceptors only at high CO<inf>2</inf>

Ventilatory and intrapulmonary chemoreceptor sensitivity to CO<inf>2</inf> in the burrowing owl

Acid-base balance during lactic acid infusion in the lizard varanus salvator

Exercise hyperpnea in the duck without intrapulmonary chemoreceptor involvement

The influence of alkalosis on panting

Response of intrapulmonary chemoreceptors in the duck to changes in PCO2 and pH

Abstract

Respir. Physiol.

J. Biol. Chem.

Respir. Physiol.

Respir. Physiol.

Respir. Physiol.

Respir. Physiol.

Respir. Physiol.

Respir. Physiol.

Respir. Physiol.

Microelectrode measurement of the intracellular pH and buffering power of mouse soleus muscle fibres

J. Physiol. (London)

Physiological parameters which determine PCO2 at the intrapulmonary chemoreceptor site in Gallus domesticus

The relationship between intracellular pH and potassium concentration in fromg brain in vivo

Bull. Europ. Physiopathol. Resp.

Response of intrapulmonary chemoreceptors in the duck to changes in P_CO₂ and pH

Physiological parameters which determine P_CO₂ at the intrapulmonary chemoreceptor site in Gallus domesticus