Initiation and Control of Chemoreceptor Activity in the Carotid Body

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Initiation and Control of Chemoreceptor Activity in the Carotid Body

Salvatore J. Fidone, Constancio Gonzalez

10.1002/cphy.cp030209

Source: Supplement 11: Handbook of Physiology, The Respiratory System, Control of Breathing

Originally published: 1986

Published online: January 2011

Full Article on Wiley Online Library

Abstract
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References

Abstract

The sections in this article are:

1 Structure

1.1 General Anatomy, Histology, and Embryology of Carotid Body

1.2 Carotid Body Ultrastructure

1.3 Pathological Changes and Physiologically Induced Changes in Carotid Body Morphology

2 Response of Chemoreceptors

2.1 Resting Chemoreceptor Discharge

2.2 Chemoreceptor Response to Hypoxia

2.3 Chemoreceptor Response to Partial Pressure of CO2 and pH

2.4 Chemoreceptor Response to Temperature and Osmolarity

2.5 Carotid Body Blood Flow, O2 Consumption, and Chemoresponse

2.6 Efferent Modulation of Chemosensory Discharge

3 Mechanisms of Chemoreception

3.1 Transducer Element(s) in Carotid Body

3.2 Biophysical Aspects of Chemoreception

3.3 Role of Putative Neurotransmitters in Chemotransduction

3.4 Hypotheses on Mechanisms of Chemoreception

4 Addendum

4.1 Recent Advances in Carotid Body Chemoreception

4.2 Structure

4.3 Response of Chemoreceptors

4.4 Mechanisms of Chemoreception

	Figure 1. Various types of cells in cat carotid body. A, afferent nerve ending; E, vascular endothelial cell; F, fibroblast; G, type I cell; P, perineurial cell; S, sheath cell (type II cell); SC, Schwann cell; SM, vascular smooth muscle cell; V, blood vessel lumen; arrows, unmyelinated axons, x13,800. Courtesy of Dr. Donald McDonald
	Figure 2. Cellular, neural, and vascular architecture of carotid body. Functional pathways are indicated (see text for detailed discussion). From Williams and Warwick 522
	Figure 3. A: averaged neural discharge (expressed as percentage of maximum asphyxie activity) from carotid bodies of 7 cats anesthetized with pentobarbital and paralyzed with gallamine in response to changing arterial O₂ tension () plotted semilogarithmically. Mean values ± 1 SD are shown for arterial pH (pHa) and arterial CO₂ tension () and slope of response curve between of 30 and 40 Torr. B: averaged neural discharge from carotid body of cat in response to changing at 2 values of but with pHa kept nearly unchanged by administration of NaHCO₃ before was increased. To provide physiological scale of response of carotid body in A and B, 0% activity has been defined as minimum level of response seen on hyperventilation with O₂, whereas 100% response is plateau of discharge occurring with transient asphyxia of animal. C: rate of chemoreceptor afferent discharges (impulses/s) in single fibers plotted against (all values from same cat). Middle graph shows 2 fibers (•, ○) from same strand; upper and lower graphs are from single fibers. Range of for upper graph, 28‐31 Torr; for middle graph, 29‐31 Torr; for lower graph, 31‐34 Torr. Mean arterial pressure ± SD for upper graph, 95 ± 7 Torr; for middle graph, 97 ± 5 Torr; for lower graph, 123 ± 6 Torr. From Hornbein 264. From Hornbein and Roos 266. From Biscoe et al. 50
	Figure 4. A: nerve discharge (impulses/s) recorded from single chemoreceptor afferent fiber plotted against arterial CO₂ tension (). For each curve, pH was kept constant. ○, pH = 7.25, mean arterial pressure ± SD = 91 ± 9 Torr. •, pH = 7.45, mean arterial pressure ± SD = 85 ± 4 Torr. Arterial O₂ tension () was 80 Torr throughout. B: discharge rate (impulses/min) recorded from single chemoreceptor afferent fiber plotted against (○, •, □) and against pH (Δ). ○, pH = 7.51‐7.54; •, pH = 7.35–7.37; ○, pH = 7.15‐7.17; Δ, = 26 Torr. Value for was 270 Torr. Some additional data not shown on other graphs were used for pH plot. From Biscoe et al. 50
	Figure 5. Threshold stimuli for single carotid chemoreceptors. Each point represents combination of arterial CO₂ () and O₂ () tensions at which receptor was just active. Clearly, threshold was lower at lower . From Lahiri 303
	Figure 6. A: 3‐dimensional graph of average carotid chemoreceptor response curves from 5 cats. Percent of maximum asphyxie response (% of MAR) is plotted as function of arterial CO₂ tension () at 4 levels of arterial O₂ tension (); it was averaged from curves for individual animals at intervals of 5 mmHg . Generally, n for “average points” is 5, but it may drop to 3 at higher values of curve. B: single chemoreceptor fiber. Response to sudden application of hypercapnic stimulus before (upper graph) and after (lower graph) inhibiting carbonic anhydrase of carotid body with acetazolamide (Diamox). From Fitzgerald and Parks 185. From Black et al. 60
	Figure 7. A: summary of O₂ tensions () found in 27 cats in which mean arterial pressure was above 70 mmHg. Surface: = 68, SE = 0.7, range = 0‐109. Deep: = 42, SE = 1.8, range = 0‐107. B: frequency distribution of tissue values in cat carotid body. On x‐axis, tissue values are divided into ranges; y‐axis shows frequency of observed values: n = 351 = 100%; = 25 Torr; median = 20 Torr. From Whalen et al. 516. From Acker et al. 7
	Figure 8. A: effects of acetylcholine (ACh; 50 μg) on membrane potential of normal (upper trace) and 6‐day‐denervated (lower trace) glomus cells impaled with micropipette filled with 6% Procion yellow. Cells identified after ejecting dye from pipette. Resting membrane potential, −52 mV. B: impalement of single nerve ending yields spontaneous depolarizing potentials (SDPs) that, if large enough, appear to evoke sensory discharges. Notice that smaller SDPs do not give rise to action potentials and that terminal was invaded by spikes originating elsewhere (collateral branches?). Nerve ending was identified by staining after recording. C: carotid body in vitro. Depolarizing potentials recorded by glass tubes filled with 3 M KCl agar separated by sucrose gap. L, Locke solution; S, sucrose. Nerve crushed (x) on right‐side L compartment. Arrows: upper trace, injection of 100 μg of ACh; middle trace, injection of 7.5‐μg of NaCN; lower trace, injection of 20‐μl of Locke solution at pH 2. Calibration: 5 mV, 10 s (top calibration for upper and middle traces, bottom calibration for lower trace). From Hayashida and Eyzaguirre 229. From Hayashida et al. 230. From Eyzaguirre et al. 150
	Figure 9. Effects of low O₂ on release of dopamine (DA) and chemoreceptor discharge recorded from rabbit carotid body during superfusion of organ in vitro. Organs were incubated for 2 h in 100% O₂‐equilibrated Tyrode's solution containing [³H]tyrosine (DA precursor) prior to experiment. Release of DA is measured as sum of [³H]DA plus ³H‐labeled 3,4‐dihydroxyphenylacetic acid (DO‐PAC; principal DA catabolite in carotid body); chemoreceptor discharge was recorded from CSN with suction electrodes. A: release of [³H]DA and efflux of [³H]DOPAC during 3 stimulus cycles of 0% O₂, 30% O₂, and 10% O₂. Each stimulus cycle consisted of 5‐min control period (superfusion with 100% O2‐equilibrated Tyrode's solution), 5‐min stimulus period (superfusion with respective stimulus gas–equilibrated Tyrode's solution), and 3 successive poststimulus collection periods (superfusion with 100% O₂‐equilibrated media). Chemoreceptor discharge during each 5‐min stimulus period is shown by insets in A. B: relationship between total [³H]DA release ([³H]DA + [³H]DOPAC), peak (max) chemoreceptor discharge, and mean chemoreceptor discharge during stimulus periods are indicated. Response ratio is net stimulus‐induced change in release or discharge (i.e., stimulated‐control/control). From Fidone et al. 169

Figure 1.

Various types of cells in cat carotid body. A, afferent nerve ending; E, vascular endothelial cell; F, fibroblast; G, type I cell; P, perineurial cell; S, sheath cell (type II cell); SC, Schwann cell; SM, vascular smooth muscle cell; V, blood vessel lumen; arrows, unmyelinated axons, x13,800.

Courtesy of Dr. Donald McDonald

Figure 2.

Cellular, neural, and vascular architecture of carotid body. Functional pathways are indicated (see text for detailed discussion).

From Williams and Warwick 522

Figure 3.

A: averaged neural discharge (expressed as percentage of maximum asphyxie activity) from carotid bodies of 7 cats anesthetized with pentobarbital and paralyzed with gallamine in response to changing arterial O₂ tension () plotted semilogarithmically. Mean values ± 1 SD are shown for arterial pH (pHa) and arterial CO₂ tension () and slope of response curve between of 30 and 40 Torr. B: averaged neural discharge from carotid body of cat in response to changing at 2 values of but with pHa kept nearly unchanged by administration of NaHCO₃ before was increased. To provide physiological scale of response of carotid body in A and B, 0% activity has been defined as minimum level of response seen on hyperventilation with O₂, whereas 100% response is plateau of discharge occurring with transient asphyxia of animal. C: rate of chemoreceptor afferent discharges (impulses/s) in single fibers plotted against (all values from same cat). Middle graph shows 2 fibers (•, ○) from same strand; upper and lower graphs are from single fibers. Range of for upper graph, 28‐31 Torr; for middle graph, 29‐31 Torr; for lower graph, 31‐34 Torr. Mean arterial pressure ± SD for upper graph, 95 ± 7 Torr; for middle graph, 97 ± 5 Torr; for lower graph, 123 ± 6 Torr.

From Hornbein 264. From Hornbein and Roos 266. From Biscoe et al. 50

Figure 4.

A: nerve discharge (impulses/s) recorded from single chemoreceptor afferent fiber plotted against arterial CO₂ tension (). For each curve, pH was kept constant. ○, pH = 7.25, mean arterial pressure ± SD = 91 ± 9 Torr. •, pH = 7.45, mean arterial pressure ± SD = 85 ± 4 Torr. Arterial O₂ tension () was 80 Torr throughout. B: discharge rate (impulses/min) recorded from single chemoreceptor afferent fiber plotted against (○, •, □) and against pH (Δ). ○, pH = 7.51‐7.54; •, pH = 7.35–7.37; ○, pH = 7.15‐7.17; Δ, = 26 Torr. Value for was 270 Torr. Some additional data not shown on other graphs were used for pH plot.

From Biscoe et al. 50

Figure 5.

Threshold stimuli for single carotid chemoreceptors. Each point represents combination of arterial CO₂ () and O₂ () tensions at which receptor was just active. Clearly, threshold was lower at lower .

From Lahiri 303

Figure 6.

A: 3‐dimensional graph of average carotid chemoreceptor response curves from 5 cats. Percent of maximum asphyxie response (% of MAR) is plotted as function of arterial CO₂ tension () at 4 levels of arterial O₂ tension (); it was averaged from curves for individual animals at intervals of 5 mmHg . Generally, n for “average points” is 5, but it may drop to 3 at higher values of curve. B: single chemoreceptor fiber. Response to sudden application of hypercapnic stimulus before (upper graph) and after (lower graph) inhibiting carbonic anhydrase of carotid body with acetazolamide (Diamox).

From Fitzgerald and Parks 185. From Black et al. 60

Figure 7.

A: summary of O₂ tensions () found in 27 cats in which mean arterial pressure was above 70 mmHg. Surface: = 68, SE = 0.7, range = 0‐109. Deep: = 42, SE = 1.8, range = 0‐107. B: frequency distribution of tissue values in cat carotid body. On x‐axis, tissue values are divided into ranges; y‐axis shows frequency of observed values: n = 351 = 100%; = 25 Torr; median = 20 Torr.

From Whalen et al. 516. From Acker et al. 7

Figure 8.

A: effects of acetylcholine (ACh; 50 μg) on membrane potential of normal (upper trace) and 6‐day‐denervated (lower trace) glomus cells impaled with micropipette filled with 6% Procion yellow. Cells identified after ejecting dye from pipette. Resting membrane potential, −52 mV. B: impalement of single nerve ending yields spontaneous depolarizing potentials (SDPs) that, if large enough, appear to evoke sensory discharges. Notice that smaller SDPs do not give rise to action potentials and that terminal was invaded by spikes originating elsewhere (collateral branches?). Nerve ending was identified by staining after recording. C: carotid body in vitro. Depolarizing potentials recorded by glass tubes filled with 3 M KCl agar separated by sucrose gap. L, Locke solution; S, sucrose. Nerve crushed (x) on right‐side L compartment. Arrows: upper trace, injection of 100 μg of ACh; middle trace, injection of 7.5‐μg of NaCN; lower trace, injection of 20‐μl of Locke solution at pH 2. Calibration: 5 mV, 10 s (top calibration for upper and middle traces, bottom calibration for lower trace).

From Hayashida and Eyzaguirre 229. From Hayashida et al. 230. From Eyzaguirre et al. 150

Figure 9.

Effects of low O₂ on release of dopamine (DA) and chemoreceptor discharge recorded from rabbit carotid body during superfusion of organ in vitro. Organs were incubated for 2 h in 100% O₂‐equilibrated Tyrode's solution containing [³H]tyrosine (DA precursor) prior to experiment. Release of DA is measured as sum of [³H]DA plus ³H‐labeled 3,4‐dihydroxyphenylacetic acid (DO‐PAC; principal DA catabolite in carotid body); chemoreceptor discharge was recorded from CSN with suction electrodes. A: release of [³H]DA and efflux of [³H]DOPAC during 3 stimulus cycles of 0% O₂, 30% O₂, and 10% O₂. Each stimulus cycle consisted of 5‐min control period (superfusion with 100% O2‐equilibrated Tyrode's solution), 5‐min stimulus period (superfusion with respective stimulus gas–equilibrated Tyrode's solution), and 3 successive poststimulus collection periods (superfusion with 100% O₂‐equilibrated media). Chemoreceptor discharge during each 5‐min stimulus period is shown by insets in A. B: relationship between total [³H]DA release ([³H]DA + [³H]DOPAC), peak (max) chemoreceptor discharge, and mean chemoreceptor discharge during stimulus periods are indicated. Response ratio is net stimulus‐induced change in release or discharge (i.e., stimulated‐control/control).

From Fidone et al. 169

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Article Title:	Initiation and Control of Chemoreceptor Activity in the Carotid Body
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Salvatore J. Fidone, Constancio Gonzalez. Initiation and Control of Chemoreceptor Activity in the Carotid Body. Compr Physiol 2011, Supplement 11: Handbook of Physiology, The Respiratory System, Control of Breathing: 247-312. First published in print 1986. doi: 10.1002/cphy.cp030209

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