Hypoxic cardiorespiratory reflexes in the facultative air-breathing fish jeju (Hoplerythrinus unitaeniatus): Role of branchial O2 chemoreceptors

Department of Physiological Sciences, Federal University of São Carlos, Via Washington Luiz, km 235, São Carlos, SP, 13565-905, Brazil.
Journal of Comparative Physiology B (Impact Factor: 2.53). 03/2010; 180(6):797-811. DOI: 10.1007/s00360-010-0461-2
Source: PubMed

ABSTRACT In one series of experiments, heart frequency (f (H)), blood pressure (P (a)), gill ventilation frequency (f ( R )), ventilation amplitude (V (AMP)) and total gill ventilation (V (TOT)) were measured in intact jeju (Hoplerythrinus unitaeniatus) and jeju with progressive denervation of the branchial branches of cranial nerves IX (glossopharyngeal) and X (vagus) without access to air. When these fish were submitted to graded hypoxia (water PO(2) approximately 140, normoxia to 17 mmHg, severe hypoxia), they increased f ( R ), V (AMP), V (TOT) and P (a) and decreased f (H). In a second series of experiments, air-breathing frequency (f (RA)), measured in fish with access to the surface, increased with graded hypoxia. In both series, bilateral denervation of all gill arches eliminated the responses to graded hypoxia. Based on the effects of internal (caudal vein, 150 microg NaCN in 0.2 mL saline) and external (buccal) injections of NaCN (500 microg NaCN in 1.0 mL water) on f (R), V (AMP), V (TOT), P (a) and f (H) we conclude that the O(2) receptors involved in eliciting changes in gill ventilation and associated cardiovascular responses are present on all gill arches and monitor the O(2) levels of both inspired water and blood perfusing the gills. We also conclude that air breathing arises solely from stimulation of branchial chemoreceptors and support the hypothesis that internal hypoxaemia is the primary drive to air breathing.

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Available from: William K Milsom, Aug 19, 2015
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    • "In studies conducted with Hoplias malabaricus (Sundin et al., 1999), Hoplias lacerdae (Micheli-Campbell et al., 2009), Hoplerythrinus unitaeniatus (Lopes et al., 2010), Colossoma macropomum (Sundin et al., 2000) and Piaractus mesopotamicus (Leite et al., 2007), fish had their local reflexes abolished by sectioning specific cranial nerves innervating gill arches. In those studies, the cranial nerves (IX to the first pair of gill arches and X for the first and other gill arches) could be accessed by a small incision in the epithelium at the dorsal end of the gill arches where they meet the roof of the opercular cavity. "
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    ABSTRACT: We evaluated the role of the first pair of gill arches in control of cardiorespiratory responses to normoxia and hypoxia in the air-breathing catfish, Clarias gariepinus. An intact group (IG) and an experimental group (EG - bilateral excision of first gill arch) were submitted to graded hypoxia, with and without access to air. The first pair of gill arches ablation reduced respiratory surface area and removed innervation by cranial nerve IX. In graded hypoxia without access to air, both groups displayed bradycardia and increased ventilatory stroke volume (VT), and the IG showed a significant increase in breathing frequency (fR). The EG exhibited very high fR in normoxia that did not increase further in hypoxia, this was linked to reduced O2 extraction from the ventilatory current (EO2) and a significantly higher critical O2 tension (PcO2) than the IG. In hypoxia with access to air only the IG showed increased air-breathing, indicating that the first pair of gill arches excision severely attenuated air-breathing responses. Both groups exhibited bradycardia before and tachycardia after air-breaths. The fH and gill ventilation amplitude (VAMP) in the EG were overall higher than the IG. External and internal NaCN injections revealed that O2 chemoreceptors mediating ventilatory hypoxic responses (fR and VT) are internally oriented. The NaCN injections indicated that fR responses were mediated by receptors predominantly in the first pair of gill arches but VT responses by receptors on all gill arches. Receptors eliciting cardiac responses were both internally and externally oriented and distributed on all gill arches or extra-branchially. Air-breathing responses were predominantly mediated by receptors in the first pair of gill arches. In conclusion, the role of the first pair of gill arches is related to: a) an elevated EO2 providing an adequate O2 uptake to maintain the aerobic metabolism during normoxia; b) a significant bradycardia and increased fAB elicited by O2 chemoreceptors externally oriented; c) increase in the ventilatory variables (fR and VAMP) stimulated by O2 chemoreceptors internally oriented. Copyright © 2015 Elsevier Inc. All rights reserved.
    Comparative biochemistry and physiology. Part A, Molecular & integrative physiology 05/2015; 187. DOI:10.1016/j.cbpa.2015.05.010 · 2.37 Impact Factor
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    • "gill ventilation (Hedrick et al., 1994). Furthermore, it suggests that the internal threshold for triggering air breaths is higher than that which triggers increases in gill ventilation, which is similar to what has been found in H . unitaeniatus (Lopes et al., 2010). "
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    ABSTRACT: This study examined mechanisms underlying cardio-respiratory acclimation to moderate sustained hypoxia (6·0 kPa for 7 days at 22° C) in the bowfin Amia calva, a facultative air-breathing fish. This level of hypoxia is slightly below the critical oxygen tension (pcrit) of A. calva denied access to air (mean ± s.e. = 9·3 ± 1·0 kPa). Before exposure to sustained hypoxia, A. calva with access to air increased air-breathing frequency on exposure to acute progressive hypoxia while A. calva without access to air increased gill-breathing frequency. Exposure to sustained hypoxia increased the gill ventilation response to acute progressive hypoxia in A. calva without access to air, regardless of whether they had access to air or not during the sustained hypoxia. Additionally, there was a decrease in Hb–O2 binding affinity in these fish. This suggests that, in A. calva, acclimation to hypoxia elicits changes that increase oxygen delivery to the gas exchange surface for oxygen uptake and reduce haemoglobin affinity to enhance oxygen delivery to the tissues.
    Journal of Fish Biology 01/2013; in press(3):n/a-n/a. DOI:10.1111/jfb.12186 · 1.73 Impact Factor
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    • "The second intriguing suggestion to arise from the data is that the receptors that give rise to air breathing in response to hypercarbia are different from those that give rise to air breathing in response to hypoxia. It has now been shown in jeju that internally oriented receptors sensing changes in O 2 levels in the blood play the predominant role in eliciting air breathing in response to hypoxia (Lopes et al., 2010). The chemoreceptors primarily involved in producing air breathing in response to hypercarbia responded specifically to changes in aquatic CO 2 (Table 8). "
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    ABSTRACT: The location (gills, oro-branchial cavity or elsewhere) and orientation (external (water) or internal (blood) sensing) of the receptors involved in reflex changes in each of the different components of the cardiorespiratory response (breathing frequency, breath amplitude, heart rate, systemic vascular resistance) to hypoxia and hypercarbia are highly variable between species of water and air breathing fish. Although not universal, the receptors involved in eliciting changes in heart rate and breathing frequency in response to hypoxia and hypercarbia tend to be restricted exclusively to the gills while those producing increases in breath amplitude are more wide spread, frequently also being found at extrabranchial sites. The distribution of the chemoreceptors sensitive to CO(2) in the gills involved in producing ventilatory responses tend to be more restricted than that of the O(2)-sensitive chemoreceptors and the specific location of the receptors involved in the various components of the cardiorespiratory response can vary from those of the O(2)-sensitive chemoreceptors.
    Respiratory Physiology & Neurobiology 07/2012; 184(3). DOI:10.1016/j.resp.2012.07.013 · 1.97 Impact Factor
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