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Peripheral Chemoreceptors and Their Sensory Neurons in Chronic States of Hypo‐ and Hyperoxygenation

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Abstract

The sections in this article are:

1 Overview: Peripheral Chemoreceptors and Sensory Neurons
2 Oxygen Continuum and Optimum
3 pHo‐pHi Relationship and CO2‐H+ Stimulus Interaction with Hypoxia: Role of Carbonic Anhydrase
3.1 CO2–H+ and Interaction with Hypoxia
3.2 Catecholamine Release and Chemosensory Nerve Discharge
4 Oxygen Delivery
4.1 Po2 vs. O2 Content
4.2 Arterial Perfusion Pressure
4.3 Carotid Body Blood Volume and Flow
5 Integrated Carotid Body and Glomus Cell
6 Oxygen and Chemoreceptive Pigments
6.1 Carbon Monoxide/Oxygen
6.2 Nitric Oxide/Oxygen
7 Chronic Hypoxia Vs. Hyperoxia
7.1 Structure
7.2 Neurotransmitters and Gene Expression
7.3 Chemosensory Nerve Function
8 Chronic Cell Depolarization
9 Efferent Control
9.1 Petrosal and Nodose Ganglia
9.2 Sympathetic Ganglia
9.3 Cyclic GMP, Vascular Smooth Muscle, Glomus Cells, Petrosal Ganglion Processes, and Innervation of Carotid Body Elements
9.4 Cobalt, Other Transition Metals, and Ca2+
10 Lifelong Hypoxia and Developmental Aspects
11 Peripheral Chemoreceptors in Cardiopulmonary and Vascular Diseases
11.1 Cardiopulmonary and Vascular Diseases
11.2 Diseases of the Glomoids
11.3 Baroreceptor vs. Peripheral Chemoreceptors
12 Perspectives
Figure 1. Figure 1.

Effects of CO2 hydration and pHo on chemosensory discharge of cat carotid body. (A) Acidic hypercapnia stimulated discharge with gradual adaptation. The same hypercapnia without changing pHo showed a similar response pattern but its magnitude was less. This means that acid pHo contributed to the response, and hypercapnia itself was a stimulus, which at least in part was due to fast intracellular hydration mediated by carbonic anhydrase. (B) To examine the idea, the foregoing tests were repeated after treating the carotid body with methazolamide (40 μM). Methazolamide reduced baseline activity, eliminated the fast initial response, and delayed and dimished the magnitude of the responses to both acidic and isohydric hypercapnia. Thus intracellular carbonic anhydrase is critical for fast response to CO2. Without fast CO2 hydration the response to isohydric hypercapnia, developed slowly, but acidic hypercapnia produced a faster and larger response, indicating a significant effect of pHo.

Figure 2. Figure 2.

Time course of effects of high Pco on the chemosensory response to hypoxia. Hypoxia of 50 torr stimulated discharge in the absence of bright light. At point a the perfusate was changed to the same hypoxia plus 300 torr Pco. The immediate effect was a depression of the activity (b), followed by excitation. The excitation was eliminated by bright light (c) (photodissociation of the CO complex) even though the same hypoxia was present. Clearly, hypoxia did not cause the usual stimulation in the presence of CO. However, undissociated CO complex elicited chemoreception.

Figure 3. Figure 3.

(A) Control cat carotid body (150 torr of inspired oxygen pressure). Two glomus cells are in view. ER, endoplasmic reticulum; M, mitochondria. There are numerous dense‐core granules and an average number of mitochondria. Bar indicates 1 μm magnification. (B) Carotid body of a chronically hypoxic cat (28 days of 70 torr inspired oxygen pressure). Parts of several glomus (G) cells and a nerve ending (N) are seen. Overabundance of mitochondria (M) in the cells and nerve ending, are apparent. Bar indicates 1 μm magnification.

Figure 4. Figure 4.

(A) Neuroglomus junction in a normal cat carotid body (150 torr of inspired oxygen pressure). Nerve ending (N) on the glomus cell (G) with a cleft between is seen. Clear‐core granules in the nerve ending are of various sizes. They are particularly concentrated at the synaptic condensations. Some of the dense‐core vesicles in the glomus cell appear to have lost their contents and are less dense. Bar indicates 0.2 μm magnification.

(B) Neuroglomus junction in a carotid body of a chronically hypoxic cat (28 days of 70 torr inspired oxygen pressure). Along the length of the synaptic junction the clear‐core vesicles (V) is arranged in concentric rings. Three such arrangements can be identified (arrows). These vesicles are gravitated toward the synapse. The dense‐core vesicles in the glomus (G) are also concentrated near one end of the synapse. Bar indicates 0.2 μm magnification.

Figure 5. Figure 5.

Effects of chronic hyperoxia on cat carotid body ultrastructure (63 h of 700 torr inspired oxygen pressure). Numerous endoplasmic reticulum (ER/er) are seen in all glomus cells. Dense‐core vesicles are preponderant, and mitochondria in glomus cells manifest low levels of cristae, unlike in another structure near the blood vessel at top. Bar indicates 1 μm magnification.

Figure 6. Figure 6.

Carotid body of a chronically hyperoxic cat at a higher magnification than Figure 5 (63 h of 700 torr inspired oxygen pressure). Membranous structures in and around glomus cells are numerous. A nerve ending (N) on a glomus (G) cell appears normal, but clear‐core vesicles are only few. Dense‐core vesicles are quite abundant but appear to be fusing in many instances. Mitochondria (M) in glomus cells show fewer cristae. There is a lipofuscin body (*) in a glomus cell. This structure appears to be a repository of some of the dense‐core vesicles. Another glomus cell shows a cilium (C). Bar indicates 1 μm magnification.

Figure 7. Figure 7.

Relationship between inspired Po2 at high altitudes and alveolar/arterial Pco2, indicating high respiratory drive in the low‐altitude native (LAN) and low respiratory drive in the high‐altitude native (HAN).

(Reprinted with permission from Santolaya et al., Respir. Physiol. 77: 253–262, 1989, see ref. 134.)


Figure 1.

Effects of CO2 hydration and pHo on chemosensory discharge of cat carotid body. (A) Acidic hypercapnia stimulated discharge with gradual adaptation. The same hypercapnia without changing pHo showed a similar response pattern but its magnitude was less. This means that acid pHo contributed to the response, and hypercapnia itself was a stimulus, which at least in part was due to fast intracellular hydration mediated by carbonic anhydrase. (B) To examine the idea, the foregoing tests were repeated after treating the carotid body with methazolamide (40 μM). Methazolamide reduced baseline activity, eliminated the fast initial response, and delayed and dimished the magnitude of the responses to both acidic and isohydric hypercapnia. Thus intracellular carbonic anhydrase is critical for fast response to CO2. Without fast CO2 hydration the response to isohydric hypercapnia, developed slowly, but acidic hypercapnia produced a faster and larger response, indicating a significant effect of pHo.



Figure 2.

Time course of effects of high Pco on the chemosensory response to hypoxia. Hypoxia of 50 torr stimulated discharge in the absence of bright light. At point a the perfusate was changed to the same hypoxia plus 300 torr Pco. The immediate effect was a depression of the activity (b), followed by excitation. The excitation was eliminated by bright light (c) (photodissociation of the CO complex) even though the same hypoxia was present. Clearly, hypoxia did not cause the usual stimulation in the presence of CO. However, undissociated CO complex elicited chemoreception.



Figure 3.

(A) Control cat carotid body (150 torr of inspired oxygen pressure). Two glomus cells are in view. ER, endoplasmic reticulum; M, mitochondria. There are numerous dense‐core granules and an average number of mitochondria. Bar indicates 1 μm magnification. (B) Carotid body of a chronically hypoxic cat (28 days of 70 torr inspired oxygen pressure). Parts of several glomus (G) cells and a nerve ending (N) are seen. Overabundance of mitochondria (M) in the cells and nerve ending, are apparent. Bar indicates 1 μm magnification.



Figure 4.

(A) Neuroglomus junction in a normal cat carotid body (150 torr of inspired oxygen pressure). Nerve ending (N) on the glomus cell (G) with a cleft between is seen. Clear‐core granules in the nerve ending are of various sizes. They are particularly concentrated at the synaptic condensations. Some of the dense‐core vesicles in the glomus cell appear to have lost their contents and are less dense. Bar indicates 0.2 μm magnification.

(B) Neuroglomus junction in a carotid body of a chronically hypoxic cat (28 days of 70 torr inspired oxygen pressure). Along the length of the synaptic junction the clear‐core vesicles (V) is arranged in concentric rings. Three such arrangements can be identified (arrows). These vesicles are gravitated toward the synapse. The dense‐core vesicles in the glomus (G) are also concentrated near one end of the synapse. Bar indicates 0.2 μm magnification.



Figure 5.

Effects of chronic hyperoxia on cat carotid body ultrastructure (63 h of 700 torr inspired oxygen pressure). Numerous endoplasmic reticulum (ER/er) are seen in all glomus cells. Dense‐core vesicles are preponderant, and mitochondria in glomus cells manifest low levels of cristae, unlike in another structure near the blood vessel at top. Bar indicates 1 μm magnification.



Figure 6.

Carotid body of a chronically hyperoxic cat at a higher magnification than Figure 5 (63 h of 700 torr inspired oxygen pressure). Membranous structures in and around glomus cells are numerous. A nerve ending (N) on a glomus (G) cell appears normal, but clear‐core vesicles are only few. Dense‐core vesicles are quite abundant but appear to be fusing in many instances. Mitochondria (M) in glomus cells show fewer cristae. There is a lipofuscin body (*) in a glomus cell. This structure appears to be a repository of some of the dense‐core vesicles. Another glomus cell shows a cilium (C). Bar indicates 1 μm magnification.



Figure 7.

Relationship between inspired Po2 at high altitudes and alveolar/arterial Pco2, indicating high respiratory drive in the low‐altitude native (LAN) and low respiratory drive in the high‐altitude native (HAN).

(Reprinted with permission from Santolaya et al., Respir. Physiol. 77: 253–262, 1989, see ref. 134.)
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Sukhamay Lahiri. Peripheral Chemoreceptors and Their Sensory Neurons in Chronic States of Hypo‐ and Hyperoxygenation. Compr Physiol 2011, Supplement 14: Handbook of Physiology, Environmental Physiology: 1183-1206. First published in print 1996. doi: 10.1002/cphy.cp040251