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Peripheral Chemoreceptors: Function and Plasticity of the Carotid Body

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Abstract

The discovery of the sensory nature of the carotid body dates back to the beginning of the 20th century. Following these seminal discoveries, research into carotid body mechanisms moved forward progressively through the 20th century, with many descriptions of the ultrastructure of the organ and stimulus‐response measurements at the level of the whole organ. The later part of 20th century witnessed the first descriptions of the cellular responses and electrophysiology of isolated and cultured type I and type II cells, and there now exist a number of testable hypotheses of chemotransduction. The goal of this article is to provide a comprehensive review of current concepts on sensory transduction and transmission of the hypoxic stimulus at the carotid body with an emphasis on integrating cellular mechanisms with the whole organ responses and highlighting the gaps or discrepancies in our knowledge. It is increasingly evident that in addition to hypoxia, the carotid body responds to a wide variety of blood‐borne stimuli, including reduced glucose and immune‐related cytokines and we therefore also consider the evidence for a polymodal function of the carotid body and its implications. It is clear that the sensory function of the carotid body exhibits considerable plasticity in response to the chronic perturbations in environmental O2 that is associated with many physiological and pathological conditions. The mechanisms and consequences of carotid body plasticity in health and disease are discussed in the final sections of this article. © 2012 American Physiological Society. Compr Physiol 2:141‐219, 2012.

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Figure 1. Figure 1.

Ultrastructure of the carotid body. (A) Reproduction of the original drawing of Fernando de Castro published in De Castro (1926), part of the Fernando de Castro Archives. Different glomeruli are shown close to the carotid artery (A). Incoming sympathetic nerve from the superior cervical ganglion (E) is a minor contribution to the innervation of the carotid body. The same can be said about the vagus nerve (LX) in the vicinity of the carotid body. By contrast, the most relevant contingent of afferents comes from the intercarotid (sinus) nerve branch of the glossopharyngeal nerve (IX). A sympathetic microganglion can be seen within the latter nerve (cg). Adapted, with permission, from by de Castro.

Figure 2. Figure 2.

Role of carotid body in ventilatory response to hypoxia. (A) Ventilatory response to progressive hypoxia in subjects after bilateral carotid body resection (BR). End tidal Po2 (PETo2) was measured by a rapid‐response O2 electrode housed in an end‐tidal sampler. PETo2 was progressively decreased at ca. 10 Torr/min, from 100 to 40 Torr. Despite advancing hypoxia, no change in ventilation was seen, as clearly reflected by unaltered profile of airway PCO2 measured by infrared CO2 analyser. Right: hypoxic ventilatory response in terms of ΔV40 (mean ± SE), that is, increment in ventilation as PETo2 decreased from 100 to 40 Torr, while PETCO2 was kept at resting level. UR, patients with unilateral carotid body resection; C, controls. ΔV40 of BR group is statistically not different from zero, whereas that of UR group is between BR and C groups. Adapted, with permission, from Honda. (B) Polygraph record of a representative trial of carotid body (CB) inhibition in a dog. The left CB was denervated prior to experiment. Perfusion of the isolated right carotid sinus region with hyperoxic (>500 mmHg) and hypocapnic (ca. 20 mmHg) blood begins at time 0 (solid vertical line). VI, ventilation; EMGdi, moving‐time‐averaged electromyogram of the costal diaphragm; VT, tidal volume; BP, blood pressure; PETCO2, end tidal PCO2; PETO2, end‐tidal Po2; and ua, arbitrary units. Interruption in the BP trace is due to blood sampling. Note that the immediate hypoventilation and PETCO2 increase with CB inhibition persists for the duration of the trial. Adapted, with permission, from Blain et al.

Figure 3. Figure 3.

Chemoafferent response to hypoxia. (A) The central, superimposed traces show an example of the increase in the frequency of action potentials, recorded from a slip of the rat carotid sinus nerve as Po2 was reduced from hyperoxia to hypoxia and then back to hyperoxia. The inset at top shows, on a different timescale, a composite of eight, superimposed action potentials. PCO2 = 38 mmHg. Adapted, with permission, from from John Wiley and Sons, Pepper et al. B. Integrated chemoreceptor response to changing arterial Po2 at one level of H+‐PCO2. Curve 1: mean arterial B.P. 130 mmHg, increasing to 160 mmHg at lowest PaO2. Adapted, with permission, from Hornbein et al.

Figure 4. Figure 4.

Effect of different levels of oxygenation upon single‐unit chemoreceptor activity in the rat in vivo. Each of the dashed lines connects the data points for a given unit (n = 20 units). Note the variation in basal discharge in normoxia, the Pao2 at the point of inflexion and the sensitivity at any PaO2, between units. The continuous line is the best fit (r2 = 0.6) for all points and represents a function in which fdis = 74010 (PaO2)−2.5, where fdis is the discharge frequency (spikes s−1) and PaO2 is recorded in mmHg. r2 is the correlation coefficient. Adapted, with permission, from John Wiley and Sons, Vidruk et al.

Figure 5. Figure 5.

Relationship between arterial and microvascular Po2 and consequence upon chemodischarge response curves. (A) Relationship between Pao2 and carotid body microvascular (CBM) Po2. O2 pressure in inspired gas was lowered in steps. At each step, Pao2, chemosensory nerve activity and phosphorescence images were measured ca. 3 min after end‐tidal gas values stabilized. Average CBM Po2 was calculated for central region of O2 pressure map of carotid body and this is plotted against measured Pao2. Top: data from six cats are presented. Each cat has a different symbol. Below: data from all six cats are fitted to single curve (line of identity also shown). (B) Relationship between Po2 (arterial and CBM) and chemosensory nerve activity. Measured values of chemosensory nerve activity in four different cats are plotted against Pao2 (open circles) and CBM Po2 (filled circles). imp/s, impulses per second. Modified, with permission, from Lahiri et al.

Figure 6. Figure 6.

Inhibition of type I cell K+ currents by hypoxia. (A) Currents from type I cells evoked by step depolarizations from −70 to +20 mV before (control), during (hypoxia), and after (wash) lowering of perfusate Po2 to 16 to 23 mmHg. The traces are representative recordings from type I cells of adult rats. (B) Mean + SEM current density‐voltage relationships before (filled circles) and during (open circles) application of hypoxic perfusate (n = 14). Modified, with permission, from John Wiley and Sons, Hatton et al.

Figure 7. Figure 7.

Effect of hypoxia upon mitochondrial membrane potential as measured by Rh 123. Top three traces: Stimulus‐response curves for three different rabbit type I cell groups. In A and B, the steady‐state maximal increase in Rh 123 fluorescence is plotted against the minimum Po2 achieved during superfusion. The trace in C shows a continuous stimulus‐response curve, as the Rh 123 fluorescence is plotted directly against the trace from a Po2 electrode placed close to the cells. Bottom trace: A continuous plot of Rh 123 fluorescence as a function of Po2 obtained from a freshly dissociated rat chromaffin cell. There was no measurable change in signal until the Po2 fell below about 5 mmHg. Modified, with permission, from John Wiley and Sons, Duchen and Biscoe.

Figure 8. Figure 8.

Relation between hypoxia and intracellular [Ca2+] in rat type I cells. (A) Effects of hypoxia on [Ca2+]i in rat type I cells. Plot of the mean [Ca2+]i against Po2 for 15 recordings.; error bars are ± SEM (for each level of Po2 in each recording [Ca2+]i was averaged over a 1 min period). Continuous line is the best fit to a hyperbolic function of form [Ca2+]i = (a + c) – [(a Po2)/(b + Po2)]; where a = 820 nM, b = 2.47 Torr, and c = 54.8 nM. Inset shows averaged (n = 15) [Ca2+]i responses to three levels of hypoxia. (B) Simultaneous recordings of membrane potential and current (using the perforated‐patch recording technique) and [Ca2+]I in a single, isolated type I cell. (i) Shows [Ca2+]i, (ii) membrane potential (Em), and (iii) current (Im; current is averaged over 10 ms intervals). The experiment begins in voltage recording mode (i.e., current clamp with I = 0; noise in current trace during voltage recording is artefactual). Inset shows action potentials recorded during anoxia on a faster time base. After the first exposure to anoxia the cell is voltage clamped at approximately −60 mV (see change in voltage trace). A second exposure to anoxia is then given. Modified, with permission, from John Wiley and Sons, Buckler and Vaughan‐Jones.

Figure 9. Figure 9.

Effect of cadmium on calcium currents and stimulus induced secretion of labeled catecholamine, [3H]CA. (A) Normalized I‐V relationships obtained in isolated chemoreceptor cells before (open circles) and during (filled circles) superfusion with 200 μM CdCl2 (n = 4). From a holding potential of −80 mV, currents were elicited by 20 ms depolarizing pulses in 10 mV intervals. On the right, single currents obtained in a representative cell in both conditions. (B) General protocol used in the experiments of [3H]CA release. The figure shows the actual release of [3H]CA (c.p.m) from a control carotid body (CB; left panel) incubated in normoxia, a 20% O2‐, 5% CO2‐, and 75% N2‐equilibrated solution (Po2 ca. 150 mmHg; open bars), or hypoxia, a 7% O2‐, 5% CO2‐, and 88% N2‐equilibrated solution (Po2 ca. 46 mmHg; gray bars). Hypoxia was applied twice (S1 and S2). Evoked release in every application of hypoxic stimuli corresponds to the sum of c.p.m. above dashed lines In the experimental CB (right panel), the protocol was identical except for the presence of 200 μM CdCl2 during the time indicated by the horizontal line. (C) Effect of CdCl2 (200 μM) on the evoked release induced by mild (7% O2‐equilibrated solution) and intense (2% O2‐equilibrated solution) hypoxia, hypercapnic acidosis (20% CO2‐equilibrated solution; pH 6.6), dinitrophenol (DNP; 100 μM) and 30 and 100 mM extracellular K+o. Experimental protocol as in B. For every type of stimulation, the figure shows averaged ratios of the evoked release in S2 to the evoked release in S1 (S2/S1), in control and cadmium‐treated CB (n = 5‐12 in every experimental condition, *** P<0.001). Adapted, with permission, from John Wiley and Sons, Rocher et al.

Figure 10. Figure 10.

Cystathionine γ‐lyase (CSE) localization in the mouse carotid body and carotid body responses to hypoxia and hypercapnia in CSE+/+ and CSE−/− mice. (A) CSE expression in carotid bodies from CSE+/+ and CSE−/− mice. Carotid body sections were stained with antibodies specific for CSE or tyrosine hydroxylase (TH), a marker of type I cells. (Scale bar: 20 μm). (B) Sensory response of isolated carotid bodies to hypoxia (Hx) (Po2 ca. 39 mmHg; at black bar) in CSE+/+ and CSE−/− mice. Integrated carotid body sensory activity (CB activity) is presented as impulses per second (imp/s). Superimposed action potentials from the single fiber are presented in inset. (C) Carotid body responses to graded hypoxia from CSE+/+ and CSE−/− mice, measured as the difference in response between baseline and hypoxia (D imp/s). Data are mean ±SEM of n = 24 (CSE+/+) and n = 23 (CSE−/−) fibers from eight mice each. (D) H2S levels (mean± SEM) in carotid bodies from CSE+/+ and CSE−/− mice under normoxia (NOR) and hypoxia (Hx) (Po2 ca. 40 mm Hg) from four independent experiments. (E) Example illustrating carotid body responses to CO2 (PCO2 ca. 68 mmHg; at black bar) in CSE+/+ and CSE−/− mice. (F) Average data mean (± SEM) of CO2 response from n = 24 (CSE+/+) and n = 19 (CSE−/−) fibers from eight mice in each group. *** and **, P<0.001 and <0.01 respectively; n.s. (not significant), P>0.05. Adapted, with permission, from Peng et al.

Figure 11. Figure 11.

Effect of respiratory acidosis upon pHi and chemodischarge. A comparison of the effects on intracellular pHi in the type I cell with carotid sinus nerve discharge rate (on the right: redrawn from Gray, 1968) of a simulated respiratory acidosis (i.e. increasing PCO2 at constant [HCO3]o). Adapted, with permission, from John Wiley and Sons, Buckler et al.

Figure 12. Figure 12.

Functional cocultures of rat type I cells and petrosal neurons. (A) Immunofluorescence staining of a coculture of dissociated rat petrosal neurons and carotid body type I cells. Culture was immunostained with tyrosine hydroxylase (TH) and neurofilament (NF, 68 kDa) antibodies and visualized with a fluorescein‐ and Texas Red‐conjugated secondary antibody, respectively. The two type I cell clusters are TH positive (cytoplasmic green fluorescence), and are intimately associated with NF‐positive petrosal processes (red fluorescence); nuclei of type I cells in the clusters appear dark. The single petrosal cell body is both TH and NF positive, accounting for the yellow‐orange fluorescence; note an NF‐positive pseudounipolar process leaves the petrosal cell body and appears to bifurcate into two main branches, each of which projects to a type I cell cluster. The petrosal neuron (PN) and type I cells were together for 8 days in vitro; scale bar represents 10 μm. (B) Effects of coculture on spontaneous membrane activity recorded with the perforated‐patch technique from petrosal neurons. (i) Typical recording illustrating lack of spontaneous activity in a PN cultured without type I cells; membrane potential, indicated by the two displaced continuous traces remained relatively steady over time. Note in i‐iii the right end of the top trace is continuous with the beginning (left end) of the lower trace. (ii) In coculture, atypical PN that was juxtaposed to a type I cell cluster showed spontaneous spikes and subthreshold potentials (two displaced traces), resembling excitatory post‐synaptic potential (EPSPs) seem at chemical synapses. (iii) Perfusion of tetrodotoxin (TTX) (1 μM) to block action potentials, did not eliminate subthreshold potentials (SSPs) recorded in a different PN, juxtaposed to a type I cell cluster. Vertical scale bar (top left) represents 20 mV; horizontal bar represents 1 s in (i) and (ii) and 1.5 s in (iii). The resting membrane potential was −65 mV in (i), −60 mV in (ii), and −70 mV in (iii). Modified, with permission, from John Wiley and Sons, Zhong et al.

Figure 13. Figure 13.

Ventilatory response to chronic hypoxia. Ventilatory responses during and after prolonged hypoxic exposures include hypoxic ventilatory decline (HVD), ventilatory acclimatization to hypoxia (VAH), and hypoxic desensitization (HD). Modified, with permission, from, Copyright Elsevier, Powell et al.

Figure 14. Figure 14.

Chemoafferent and ventilatory responses to hypoxia in HIF‐1α deficient mice. (A) Sensory responses to hypoxia (black bars) in wild type (Hif1a+/+; left panel) and HIF‐1α deficient (Hif1a+/−; right panel) mice. Po2 = partial pressure of O2 in the perfusate. Superimposed action potential of “single” fiber from which the data were derived is shown (inset). Note the blunted carotid body response to acute hypoxia in HIF‐1α deficient mice. Adapted, with permission, from John Wiley and Sons, Peng et al. (B) Effect of chronic hypoxia on ventilatory response to acute hypoxia in wild type (Hif1a+/+) (left panel) and HIF‐1α deficient (Hif1a+/−; right panel) mice. Changes in minute ventilation (VE) are expressed (mean ± SEM) relative to the values obtained while breathing 100% O2. Note the absence of ventilatory adaptation to hypoxia (VAH) in HIF‐1α deficient mice. Modified, with permission, from Kline et al.

Figure 15. Figure 15.

Effect of intermittent hypoxia upon chemodischarge. (A) Representative tracings showing the changes in carotid body sensory discharges [impulses/second (imp/s)] in response to hypoxia in a control rat and a rat conditioned with 10 days of intermittent hypoxia (IH). AP, raw action potentials; time calibration = 40 s. Hypoxic challenges are marked under the tracings as solid bars, and arterial Po2 (Pao2) levels during hypoxic challenges are indicated under the bars. Inset: setting of the window discriminator for selection of action potentials above the baseline. (B) Average data showing the relationships of carotid body (CB) sensory activity (expressed as % of asphyxia response) against Pao2 while arterial PCO2 (PaCO2) was maintained close to 35 Torr in control (n = 8,), IH‐conditioned (n = 8,), and recovered rats (IH‐normoxia, n = 7) that were conditioned with 10 days of IH followed by 10 days of normoxic exposure. *** P < 0.001, significantly different compared with control rats. Adapted, with permission, from Peng and Prabhakar.

Figure 16. Figure 16.

Acute intermittent hypoxia (AIH) induces sensory long term facilitation (LTF) in the carotid body in chronic intermittent hypoxia (CIH) animals. (A) Carotid body sensory activity in a control (upper) and CIH‐conditioned (lower) animal. Pre‐AIH is baseline activity; AIH #1 and AIH #10 represent the first and 10th episodes of AIH; impulses (Imp) per s, integrated sensory discharge; A.P., action potentials. (B) Average changes in the sensory activity during AIH and during every 5 min of the post‐AIH period. Average data represent mean ± SEM from control (n = 7) and 10 days CIH‐conditioned (n = 7) animals. The shaded area represents the difference in baseline activity in CIH and control animals during the post‐AIH period. Adapted, with permission, from Peng et al.

Figure 17. Figure 17.

Effect of CIH upon the cardiorespiratory system. Schematic illustration of the mechanisms and the consequences of chronic intermittent hypoxia (CIH)‐induced changes in the carotid body on cardiorespiratory systems. Adapted, with permission, from , Copyright Elsevier, Prabhakar et al.

Figure 18. Figure 18.

Effect of chronic heart failure of chemodischarge. Representative recordings of afferent discharge of carotid body (CB) chemoreceptors during normoxia and two levels of isocapnic hypoxia from a sham (left) and a chronic heart failure (CHF) rabbit (right). Adapted, with permission, from, Sun et al.



Figure 1.

Ultrastructure of the carotid body. (A) Reproduction of the original drawing of Fernando de Castro published in De Castro (1926), part of the Fernando de Castro Archives. Different glomeruli are shown close to the carotid artery (A). Incoming sympathetic nerve from the superior cervical ganglion (E) is a minor contribution to the innervation of the carotid body. The same can be said about the vagus nerve (LX) in the vicinity of the carotid body. By contrast, the most relevant contingent of afferents comes from the intercarotid (sinus) nerve branch of the glossopharyngeal nerve (IX). A sympathetic microganglion can be seen within the latter nerve (cg). Adapted, with permission, from by de Castro.



Figure 2.

Role of carotid body in ventilatory response to hypoxia. (A) Ventilatory response to progressive hypoxia in subjects after bilateral carotid body resection (BR). End tidal Po2 (PETo2) was measured by a rapid‐response O2 electrode housed in an end‐tidal sampler. PETo2 was progressively decreased at ca. 10 Torr/min, from 100 to 40 Torr. Despite advancing hypoxia, no change in ventilation was seen, as clearly reflected by unaltered profile of airway PCO2 measured by infrared CO2 analyser. Right: hypoxic ventilatory response in terms of ΔV40 (mean ± SE), that is, increment in ventilation as PETo2 decreased from 100 to 40 Torr, while PETCO2 was kept at resting level. UR, patients with unilateral carotid body resection; C, controls. ΔV40 of BR group is statistically not different from zero, whereas that of UR group is between BR and C groups. Adapted, with permission, from Honda. (B) Polygraph record of a representative trial of carotid body (CB) inhibition in a dog. The left CB was denervated prior to experiment. Perfusion of the isolated right carotid sinus region with hyperoxic (>500 mmHg) and hypocapnic (ca. 20 mmHg) blood begins at time 0 (solid vertical line). VI, ventilation; EMGdi, moving‐time‐averaged electromyogram of the costal diaphragm; VT, tidal volume; BP, blood pressure; PETCO2, end tidal PCO2; PETO2, end‐tidal Po2; and ua, arbitrary units. Interruption in the BP trace is due to blood sampling. Note that the immediate hypoventilation and PETCO2 increase with CB inhibition persists for the duration of the trial. Adapted, with permission, from Blain et al.



Figure 3.

Chemoafferent response to hypoxia. (A) The central, superimposed traces show an example of the increase in the frequency of action potentials, recorded from a slip of the rat carotid sinus nerve as Po2 was reduced from hyperoxia to hypoxia and then back to hyperoxia. The inset at top shows, on a different timescale, a composite of eight, superimposed action potentials. PCO2 = 38 mmHg. Adapted, with permission, from from John Wiley and Sons, Pepper et al. B. Integrated chemoreceptor response to changing arterial Po2 at one level of H+‐PCO2. Curve 1: mean arterial B.P. 130 mmHg, increasing to 160 mmHg at lowest PaO2. Adapted, with permission, from Hornbein et al.



Figure 4.

Effect of different levels of oxygenation upon single‐unit chemoreceptor activity in the rat in vivo. Each of the dashed lines connects the data points for a given unit (n = 20 units). Note the variation in basal discharge in normoxia, the Pao2 at the point of inflexion and the sensitivity at any PaO2, between units. The continuous line is the best fit (r2 = 0.6) for all points and represents a function in which fdis = 74010 (PaO2)−2.5, where fdis is the discharge frequency (spikes s−1) and PaO2 is recorded in mmHg. r2 is the correlation coefficient. Adapted, with permission, from John Wiley and Sons, Vidruk et al.



Figure 5.

Relationship between arterial and microvascular Po2 and consequence upon chemodischarge response curves. (A) Relationship between Pao2 and carotid body microvascular (CBM) Po2. O2 pressure in inspired gas was lowered in steps. At each step, Pao2, chemosensory nerve activity and phosphorescence images were measured ca. 3 min after end‐tidal gas values stabilized. Average CBM Po2 was calculated for central region of O2 pressure map of carotid body and this is plotted against measured Pao2. Top: data from six cats are presented. Each cat has a different symbol. Below: data from all six cats are fitted to single curve (line of identity also shown). (B) Relationship between Po2 (arterial and CBM) and chemosensory nerve activity. Measured values of chemosensory nerve activity in four different cats are plotted against Pao2 (open circles) and CBM Po2 (filled circles). imp/s, impulses per second. Modified, with permission, from Lahiri et al.



Figure 6.

Inhibition of type I cell K+ currents by hypoxia. (A) Currents from type I cells evoked by step depolarizations from −70 to +20 mV before (control), during (hypoxia), and after (wash) lowering of perfusate Po2 to 16 to 23 mmHg. The traces are representative recordings from type I cells of adult rats. (B) Mean + SEM current density‐voltage relationships before (filled circles) and during (open circles) application of hypoxic perfusate (n = 14). Modified, with permission, from John Wiley and Sons, Hatton et al.



Figure 7.

Effect of hypoxia upon mitochondrial membrane potential as measured by Rh 123. Top three traces: Stimulus‐response curves for three different rabbit type I cell groups. In A and B, the steady‐state maximal increase in Rh 123 fluorescence is plotted against the minimum Po2 achieved during superfusion. The trace in C shows a continuous stimulus‐response curve, as the Rh 123 fluorescence is plotted directly against the trace from a Po2 electrode placed close to the cells. Bottom trace: A continuous plot of Rh 123 fluorescence as a function of Po2 obtained from a freshly dissociated rat chromaffin cell. There was no measurable change in signal until the Po2 fell below about 5 mmHg. Modified, with permission, from John Wiley and Sons, Duchen and Biscoe.



Figure 8.

Relation between hypoxia and intracellular [Ca2+] in rat type I cells. (A) Effects of hypoxia on [Ca2+]i in rat type I cells. Plot of the mean [Ca2+]i against Po2 for 15 recordings.; error bars are ± SEM (for each level of Po2 in each recording [Ca2+]i was averaged over a 1 min period). Continuous line is the best fit to a hyperbolic function of form [Ca2+]i = (a + c) – [(a Po2)/(b + Po2)]; where a = 820 nM, b = 2.47 Torr, and c = 54.8 nM. Inset shows averaged (n = 15) [Ca2+]i responses to three levels of hypoxia. (B) Simultaneous recordings of membrane potential and current (using the perforated‐patch recording technique) and [Ca2+]I in a single, isolated type I cell. (i) Shows [Ca2+]i, (ii) membrane potential (Em), and (iii) current (Im; current is averaged over 10 ms intervals). The experiment begins in voltage recording mode (i.e., current clamp with I = 0; noise in current trace during voltage recording is artefactual). Inset shows action potentials recorded during anoxia on a faster time base. After the first exposure to anoxia the cell is voltage clamped at approximately −60 mV (see change in voltage trace). A second exposure to anoxia is then given. Modified, with permission, from John Wiley and Sons, Buckler and Vaughan‐Jones.



Figure 9.

Effect of cadmium on calcium currents and stimulus induced secretion of labeled catecholamine, [3H]CA. (A) Normalized I‐V relationships obtained in isolated chemoreceptor cells before (open circles) and during (filled circles) superfusion with 200 μM CdCl2 (n = 4). From a holding potential of −80 mV, currents were elicited by 20 ms depolarizing pulses in 10 mV intervals. On the right, single currents obtained in a representative cell in both conditions. (B) General protocol used in the experiments of [3H]CA release. The figure shows the actual release of [3H]CA (c.p.m) from a control carotid body (CB; left panel) incubated in normoxia, a 20% O2‐, 5% CO2‐, and 75% N2‐equilibrated solution (Po2 ca. 150 mmHg; open bars), or hypoxia, a 7% O2‐, 5% CO2‐, and 88% N2‐equilibrated solution (Po2 ca. 46 mmHg; gray bars). Hypoxia was applied twice (S1 and S2). Evoked release in every application of hypoxic stimuli corresponds to the sum of c.p.m. above dashed lines In the experimental CB (right panel), the protocol was identical except for the presence of 200 μM CdCl2 during the time indicated by the horizontal line. (C) Effect of CdCl2 (200 μM) on the evoked release induced by mild (7% O2‐equilibrated solution) and intense (2% O2‐equilibrated solution) hypoxia, hypercapnic acidosis (20% CO2‐equilibrated solution; pH 6.6), dinitrophenol (DNP; 100 μM) and 30 and 100 mM extracellular K+o. Experimental protocol as in B. For every type of stimulation, the figure shows averaged ratios of the evoked release in S2 to the evoked release in S1 (S2/S1), in control and cadmium‐treated CB (n = 5‐12 in every experimental condition, *** P<0.001). Adapted, with permission, from John Wiley and Sons, Rocher et al.



Figure 10.

Cystathionine γ‐lyase (CSE) localization in the mouse carotid body and carotid body responses to hypoxia and hypercapnia in CSE+/+ and CSE−/− mice. (A) CSE expression in carotid bodies from CSE+/+ and CSE−/− mice. Carotid body sections were stained with antibodies specific for CSE or tyrosine hydroxylase (TH), a marker of type I cells. (Scale bar: 20 μm). (B) Sensory response of isolated carotid bodies to hypoxia (Hx) (Po2 ca. 39 mmHg; at black bar) in CSE+/+ and CSE−/− mice. Integrated carotid body sensory activity (CB activity) is presented as impulses per second (imp/s). Superimposed action potentials from the single fiber are presented in inset. (C) Carotid body responses to graded hypoxia from CSE+/+ and CSE−/− mice, measured as the difference in response between baseline and hypoxia (D imp/s). Data are mean ±SEM of n = 24 (CSE+/+) and n = 23 (CSE−/−) fibers from eight mice each. (D) H2S levels (mean± SEM) in carotid bodies from CSE+/+ and CSE−/− mice under normoxia (NOR) and hypoxia (Hx) (Po2 ca. 40 mm Hg) from four independent experiments. (E) Example illustrating carotid body responses to CO2 (PCO2 ca. 68 mmHg; at black bar) in CSE+/+ and CSE−/− mice. (F) Average data mean (± SEM) of CO2 response from n = 24 (CSE+/+) and n = 19 (CSE−/−) fibers from eight mice in each group. *** and **, P<0.001 and <0.01 respectively; n.s. (not significant), P>0.05. Adapted, with permission, from Peng et al.



Figure 11.

Effect of respiratory acidosis upon pHi and chemodischarge. A comparison of the effects on intracellular pHi in the type I cell with carotid sinus nerve discharge rate (on the right: redrawn from Gray, 1968) of a simulated respiratory acidosis (i.e. increasing PCO2 at constant [HCO3]o). Adapted, with permission, from John Wiley and Sons, Buckler et al.



Figure 12.

Functional cocultures of rat type I cells and petrosal neurons. (A) Immunofluorescence staining of a coculture of dissociated rat petrosal neurons and carotid body type I cells. Culture was immunostained with tyrosine hydroxylase (TH) and neurofilament (NF, 68 kDa) antibodies and visualized with a fluorescein‐ and Texas Red‐conjugated secondary antibody, respectively. The two type I cell clusters are TH positive (cytoplasmic green fluorescence), and are intimately associated with NF‐positive petrosal processes (red fluorescence); nuclei of type I cells in the clusters appear dark. The single petrosal cell body is both TH and NF positive, accounting for the yellow‐orange fluorescence; note an NF‐positive pseudounipolar process leaves the petrosal cell body and appears to bifurcate into two main branches, each of which projects to a type I cell cluster. The petrosal neuron (PN) and type I cells were together for 8 days in vitro; scale bar represents 10 μm. (B) Effects of coculture on spontaneous membrane activity recorded with the perforated‐patch technique from petrosal neurons. (i) Typical recording illustrating lack of spontaneous activity in a PN cultured without type I cells; membrane potential, indicated by the two displaced continuous traces remained relatively steady over time. Note in i‐iii the right end of the top trace is continuous with the beginning (left end) of the lower trace. (ii) In coculture, atypical PN that was juxtaposed to a type I cell cluster showed spontaneous spikes and subthreshold potentials (two displaced traces), resembling excitatory post‐synaptic potential (EPSPs) seem at chemical synapses. (iii) Perfusion of tetrodotoxin (TTX) (1 μM) to block action potentials, did not eliminate subthreshold potentials (SSPs) recorded in a different PN, juxtaposed to a type I cell cluster. Vertical scale bar (top left) represents 20 mV; horizontal bar represents 1 s in (i) and (ii) and 1.5 s in (iii). The resting membrane potential was −65 mV in (i), −60 mV in (ii), and −70 mV in (iii). Modified, with permission, from John Wiley and Sons, Zhong et al.



Figure 13.

Ventilatory response to chronic hypoxia. Ventilatory responses during and after prolonged hypoxic exposures include hypoxic ventilatory decline (HVD), ventilatory acclimatization to hypoxia (VAH), and hypoxic desensitization (HD). Modified, with permission, from, Copyright Elsevier, Powell et al.



Figure 14.

Chemoafferent and ventilatory responses to hypoxia in HIF‐1α deficient mice. (A) Sensory responses to hypoxia (black bars) in wild type (Hif1a+/+; left panel) and HIF‐1α deficient (Hif1a+/−; right panel) mice. Po2 = partial pressure of O2 in the perfusate. Superimposed action potential of “single” fiber from which the data were derived is shown (inset). Note the blunted carotid body response to acute hypoxia in HIF‐1α deficient mice. Adapted, with permission, from John Wiley and Sons, Peng et al. (B) Effect of chronic hypoxia on ventilatory response to acute hypoxia in wild type (Hif1a+/+) (left panel) and HIF‐1α deficient (Hif1a+/−; right panel) mice. Changes in minute ventilation (VE) are expressed (mean ± SEM) relative to the values obtained while breathing 100% O2. Note the absence of ventilatory adaptation to hypoxia (VAH) in HIF‐1α deficient mice. Modified, with permission, from Kline et al.



Figure 15.

Effect of intermittent hypoxia upon chemodischarge. (A) Representative tracings showing the changes in carotid body sensory discharges [impulses/second (imp/s)] in response to hypoxia in a control rat and a rat conditioned with 10 days of intermittent hypoxia (IH). AP, raw action potentials; time calibration = 40 s. Hypoxic challenges are marked under the tracings as solid bars, and arterial Po2 (Pao2) levels during hypoxic challenges are indicated under the bars. Inset: setting of the window discriminator for selection of action potentials above the baseline. (B) Average data showing the relationships of carotid body (CB) sensory activity (expressed as % of asphyxia response) against Pao2 while arterial PCO2 (PaCO2) was maintained close to 35 Torr in control (n = 8,), IH‐conditioned (n = 8,), and recovered rats (IH‐normoxia, n = 7) that were conditioned with 10 days of IH followed by 10 days of normoxic exposure. *** P < 0.001, significantly different compared with control rats. Adapted, with permission, from Peng and Prabhakar.



Figure 16.

Acute intermittent hypoxia (AIH) induces sensory long term facilitation (LTF) in the carotid body in chronic intermittent hypoxia (CIH) animals. (A) Carotid body sensory activity in a control (upper) and CIH‐conditioned (lower) animal. Pre‐AIH is baseline activity; AIH #1 and AIH #10 represent the first and 10th episodes of AIH; impulses (Imp) per s, integrated sensory discharge; A.P., action potentials. (B) Average changes in the sensory activity during AIH and during every 5 min of the post‐AIH period. Average data represent mean ± SEM from control (n = 7) and 10 days CIH‐conditioned (n = 7) animals. The shaded area represents the difference in baseline activity in CIH and control animals during the post‐AIH period. Adapted, with permission, from Peng et al.



Figure 17.

Effect of CIH upon the cardiorespiratory system. Schematic illustration of the mechanisms and the consequences of chronic intermittent hypoxia (CIH)‐induced changes in the carotid body on cardiorespiratory systems. Adapted, with permission, from , Copyright Elsevier, Prabhakar et al.



Figure 18.

Effect of chronic heart failure of chemodischarge. Representative recordings of afferent discharge of carotid body (CB) chemoreceptors during normoxia and two levels of isocapnic hypoxia from a sham (left) and a chronic heart failure (CHF) rabbit (right). Adapted, with permission, from, Sun et al.

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Prem Kumar, Nanduri R. Prabhakar. Peripheral Chemoreceptors: Function and Plasticity of the Carotid Body. Compr Physiol 2012, 2: 141-219. doi: 10.1002/cphy.c100069