Mark L. Burleson

7 Afferent Inputs Associated with Cardioventilatory Control in Fish

Publisher Summary This chapter describes the afferent inputs associated with cardioventilatory control in fish. The basic respiratory rhythm and rhythmic contractions of the heart result from the actions of endogenous rhythm generators and do not require afferent feedback for their initiation or maintenance in fish. Mechanoreceptors sensitive to displacement of the pharynx, pharyngeal pads, gill arches, gill rakers and filaments, and air-breathing organs have been identified in fishes. As in other vertebrates, these mechanoreceptors appear to be simple free nerve endings located in connective tissue or muscle. There is direct and indirect evidence that indicates that some fishes may possess intracardiac receptors homologous to mammalian atrial and ventricular stretch receptors. The internally oriented chemoreceptors respond to the mixed venous blood somewhere between the ventral aorta and the afferent filamental artery. Nociceptors with characteristics similar to juxtapulmonary receptors in mammalian lungs have been demonstrated in the gills of dogfish.

Evidence for two oxygen-sensitive chemoreceptor loci in channel catfish, Ictalurus punctatus

Sodium cyanide (NaCN) was used as a chemical probe to help localize externally and internally oriented oxygen-Sensitive chemoreceptors and to identify the reflex effects they control in anesthetized, spontaneously breathing channel catfish (Ictalurus punctatus). Fish responded rapidly to NaCN (500μg) given in the inspired water flow (external NaCN) with transient bradycardia and a more prolonged stimulation of gill ventilation frequency (fg) and opercularpressure amplitude (POP). Internal injections of NaCN (50 μg), given via the dorsal aorta, stimulated fg and POP after about a 42-s latency but had no effect on heart rate (fb). Injections of NaCN (50 μg) into the ventral aorta significantly reduced the latency of response, stimulating POP and fg in 9–16s. Cardiovascular and ventilatory variables returned topreinjection levels within 30 min. These results suggest that cardiovascular and ventilatory reflex responses to hypoxia in channel catfish are mediated by both externally and internally oriented O₂-sensitive chemoreceptors. Externally oriented chemoreceptors appear to monitor the O2 tension of the inspired water and elicit bradycardia and hyperpnea when stimulated by aquatic hypoxia or external NaCN. Internal O2-sensitive chemoreceptors appear to respond to changes in blood O2 stimulus levels, in orjust downstream from the gills, and reflexively increase gill ventilation when stimulated by hypoxemia.

Branchial chemoreceptors mediate ventilatory responses to hypercapnic acidosis in channel catfish.

The effects of hyperoxic hypercapnia on cardiovascular and ventilatory variables and blood gas and acid/base parameters were examined in conscious and anesthetized spontaneously breathing (ASB) channel catfish, Ictalurus punctatus. These separate experiments were designed to determine: (1) if channel catfish show a ventilatory response to hypercapnic acidosis when blood O(2) content is maintained in conscious animals; and (2) whether branchial receptors innervated by cranial nerves IX and X mediate this response. The combination of high O(2) and CO(2) tensions allowed the cardioventilatory effects of hypercapnic acidosis to be assessed independently of Root or Bohr mediated changes in blood O(2) content. In the absence of significant changes in dorsal or ventral aorta O(2) content, hyperoxic hypercapnia significantly stimulated ventilation, relative to hyperoxic exposure. Hypercapnic acidosis, however, had no significant effects on blood pressure or heart rate. Branchial denervation in ASB fish abolished the ventilatory response to hypercapnic acidosis. The results indicate that hypercapnic acidosis independently stimulates ventilation in channel catfish. This response is mediated by CO(2)/pH-sensitive branchial receptors innervated by cranial nerves IX and X.

Cardioventilatory effects of acclimatization to aquatic hypoxia in channel catfish

The mechanisms responsible for altering cardioventilatory control in vertebrates in response to chronic hypoxia are not well understood but appear to be mediated through the oxygen-sensitive chemoreceptor pathway. Little is known about the effects of chronic hypoxia on cardioventilatory control in vertebrates other than mammals. The purpose of this study was to determine how cardioventilatory control and the pattern of response is altered in channel catfish (Ictalurus punctatus) by 1 week of moderate hypoxia. Fish were acclimatized for 7 days in either normoxia (P(O(2)) approximately 150 Torr) or hypoxia (P(O(2)) approximately 75 Torr). After acclimatization, cardioventilatory, blood-gas and acid/base variables were measured during normoxia (P(O(2)) 148+/-1 Torr) then at two levels of acute (5 min) hypoxia, (P(O(2)) 72.6+/-1 and 50.4+/-0.4 Torr). Ventilation was significantly greater in hypoxic acclimatized fish as was the ventilatory sensitivity to hypoxia (Delta ventilation/Delta P(O(2))). The increase in ventilation and hypoxic sensitivity was due to increases in opercular pressure amplitude, gill ventilation frequency did not change. Heart rate was greater in hypoxic acclimatized fish but decreased in both acclimatization groups in response to acute hypoxia. Heart rate sensitivity to hypoxia (Delta heart rate/Delta P(O(2))) was not affected by hypoxic acclimatization. The ventilatory effects of hypoxic acclimatization can be explained by increased sensitivity to oxygen but the effects on heart rate cannot.

Identification of central mechanisms vital for breathing in the channel catfish, Ictalurus punctatus.

To investigate central respiratory control mechanisms in channel catfish, microinjections of kainic acid (causing chemical lesion of neurons) or kynurenic acid (an antagonist of N-methyl-D-aspartate (NMDA), kainate and alpha-amino-3-OH-5-methyl-4-isooxazole-propionic-acid (AMPA) receptors) were made into the general visceral nucleus (nGV) of the medulla in anaesthetised spontaneously breathing animals. Kainic acid abolished the ventilatory movements, indicating that neurons in the nGV are crucial for maintaining normal breathing. Kynurenic acid did not affect normal breathing, but abolished the ventilatory responses to hypoxia, showing that ionotropic glutamate receptors in the nGV are vital for the production of oxygen chemoreceptor activated respiratory reflexes. In addition, immunohistochemistry of brain slices showed that interneurons and nerve fibres in the nGV display NMDA-immunoreactivity, which corroborates the physiological experiments. The results of this study suggest that neurons and glutamatergic pathways in the nGV are essential for ventilatory functions and hypoxic reflexes in channel catfish.

Central nervous control of gill filament muscles in channel catfish.

The gills of fish are innervated by cranial nerves IX and X. There have been a number of studies on the characteristics of sensory activity carried by these nerves but remarkably little is known about motor control of the gills. Efferent, motor activity to the first gill arch was recorded from the glossopharyngeal nerve in spontaneously breathing channel catfish, Ictalurus punctatus. This study addressed two objectives. The first objective was to characterize efferent branchial nerve activity in spontaneously breathing fish. Nerve recordings show bursts of activity firing in synchrony with ventilation. These bursts occurred once during either abduction or adduction of the operculum with each breath. The observed patterns of neural activity indicate that it represents motor control of gill filament abductor and adductor muscles. The data show that rhythmic output from a central pattern generator controls filament musculature during the ventilatory cycle. The second objective was to use this efferent branchial nerve activity as an index of ventilation (fictive ventilation) in fish before and after paralysis to determine if feedback from phasic mechanoreceptors affects ventilatory timing. Breath-to-breath intervals measured before and after paralysis with gallamine were not significantly different, demonstrating that rhythmic feedback from phasic mechanoreceptors in the gills and/or ventilatory musculature is not involved in the breath-to-breath timing of the normal ventilatory cycle. During the course of these experiments many fish exhibited coughing. Coughs were characterized by a distinctive pattern of nerve activity that was not altered by paralysis. Overall, the data indicate that phasic mechanoreceptor feedback during normal breathing has no effect on the pattern of central motor control of gill filament muscles.

Chapter 1 Oxygen availability: sensory systems

Publisher Summary To maintain oxidative metabolism active animals must be able to sense and respond to changes in environmental O 2 availability and metabolic O 2 demand. This is especially true for aquatic animals such as fish because they are subject to extreme spatial and temporal changes in ambient or environmental O 2 tensions. In addition, energetic activities (i.e., migration, pursuing prey, and fleeing predators) require that fishes regulate the delivery of O 2 internally to metabolically active tissues. This chapter focuses on chemoreceptors that are sensitive to O 2 and alter the performance of fishs cardiovascular and ventilatory systems to maintain oxidative metabolism in the face of decreasing environmental O 2 availability, compromised O 2 uptake ability and/or increased metabolic demand. Most experimental evidence indicates that cardiovascular and ventilatory functions are predominately driven by O 2 in aquatic animals. Carbon dioxide (CO 2 ) also appears to have direct effects on cardioventilatory reflexes in teleost fishes and elasmobranchs but these effects are more variable and less intense than the responses to O 2 .