Phenomenon of the complete suppression of cardiac activity in the Black Sea scorpionfish Scorpaena porcus (Scorpaenidae) during an alertness reaction
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Abstract
Teleosts serve as experimental models for the physiological and pathophysiological processes investigation, in particular those related to the heart work. Methods allowing to analyze the frequency parameters of the heart functioning over a long period of time require taking into account the peculiarities of fish behavioral reactions, that can affect the results of the experiment. The aim of this study was to examine the effect of the simplest test loading (sound stimulus) on the frequency parameters of the heart activity recorded by the fiber-optic method. The objects of the study were adults of Scorpaena porcus (12–15 cm long, 80–120 g in weight). In the course of experiments, each scorpionfish was kept in a separate aquarium with seawater (400×400×350 mm), with constant temperature (21 ± 0.5) °C and given oxygen content (5.5–6.7 mg·L−1, normoxia). The heart rate (HR) recording was carried out by an invasive fiber-optic method, the essence of which is to transmit the radiation of the infrared semiconductor laser of the photoplethysmograph through a thin fiber-optic cable to the pericardial membrane of the heart and then to fix the signal reflected from the contracting myocardium in the photodetector. During implantation of the photoplethysmograph light guides, the fish were anesthetized by placing them in an anesthetic solution (urethane, 2.4 g·L−1 of seawater). In the fornix of the opercular cavity above the area of the conditional heart projection, a minimal dissection of the lining epithelium was performed, through which the underlying tissues were sequentially separated by a blunt method until the pericardial membrane was reached without breaking it. Through the lumen formed in the tissues, two optical light guide sensors were introduced to the surface of the pericardial membrane. Further, free-swimming scorpionfish participated in the experiment after a day of rehabilitation after the surgery. Additionally, we assessed the functional state of the animals by visual fixation of respiratory activity by the quantity of movements of the opercular covers per minute. During studying the test loading effect on the correct registration of the scorpionfish HR, the phenomenon of temporary complete suppression of cardiac activity was revealed, which manifested itself upon presentation of sound stimuli (alertness, “freezing” reaction). The duration of cardiac arrest was 31 to 50 seconds; it was accompanied by the cessation of movement of the opercular covers (respiratory arrest, apnea). During the restoration of cardiac activity, two types of physiological reactions were noted. The first type of recovery reaction was characterized by a simultaneous 1.5-fold increase in the HR and a 2-fold enhancement in the photoplethysmograph signal amplitude. The second type of reaction was accompanied by a rise in the HR by 22 % (p < 0.05) against the backdrop of a decrement in the signal amplitude of the photoplethysmograph sensors by 28 % (p < 0.05); within 120 seconds, the scorpionfish HR returned to baseline. It is assumed that the short-term delay in the scorpionfish cardiac activity is based on the phenomenon of cardiorespiratory coupling and synchronization. The behavioral reaction in the form of suppression for the cardiac and simultaneously respiratory activity generation ensures the complete absence of acoustic and electrical signals, which unmask an ambush predator location, and contributes to the scorpionfish survival.
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References
Баринова Г. К., Асылбекова А. С. Этология рыб. Астана : Казахский агротехнический университет им. С. Сейфуллина, 2019. 300 с. [Barinova G. K., Asylbekova A. S. Etologiya ryb. Astana : Kazakhskii agrotekhnicheskii universitet im. S. Seifullina, 2019, 300 p. (in Russ.)]. http://repository.kazatu.kz/jspui/handle/123456789/389
Протасов В. Р. Биоакустика рыб. Москва : Наука, 1965. 208 с. [Protasov V. R. Bioakustika ryb. Moscow : Nauka, 1965, 208 p. (in Russ.)]
Протасов В. Р. Биоэлектрические поля в жизни рыб. Москва : Наука, 1972. 228 с. [Protasov V. R. Bioelektricheskie polya v zhizni ryb. Moscow : Nauka, 1972, 228 p. (in Russ.)]
Сладкова С. В., Сафронова Д. В., Холодкевич С. В. Изучение влияния изменений режимов освещённости, температуры и процесса кормления на кардиоактивность раков – биоиндикаторов в биоэлектронных системах мониторинга качества поверхностных вод // Вестник СПбГУ. Серия 3. 2016. № 1. С. 137–149. [Sladkova S. V., Safronova D. V., Kholodkevich S. V. The study of the effect of light intensity, temperature and feeding conditions changes on the cardiac activity of crayfish-bioindicators in bioelectronic systems for surface water quality monitoring. Vestnik SPbGU, Seriya 3, 2016, no. 1, pp. 137–149. (in Russ.)]
Чайковский Ю. В. Элементы эволюционной диатропики. Москва : Наука, 1990. 272 с. [Chaikovskii Yu. V. Elementy evolyutsionnoi diatropiki. Moscow : Nauka, 1990, 272 p. (in Russ.)]
Ballintijn C. M., Roberts B. L. A Hering–Breuer-type reflex from the gill arches of teleost fish. In: Exogenous and Endogenous Influences on Metabolic and Neural Control : proceedings of the third congress of the European Society for Comparative Physiology and Biochemistry, 1982, vol. 2, pp. 55–56. https://doi.org/10.1016/B978-0-08-028845-1.50036-6
Barrett D. J., Taylor E. W. The location of cardiac vagal preganglionic neurones in the brainstem of the dogfish. Journal of Experimental Biology, 1985, vol. 117, iss. 1, pp. 449–458. https://doi.org/10.1242/jeb.117.1.449
Cambell H. A., Taylor E. W., Egginton S. The use of power spectral analysis to determine cardiorespiratory control in the short-horned sculpin Myoxocephalus scorpius. Journal of Experimental Biology, 2004, vol. 207, pp. 1969–1976. https://doi.org/10.1242/jeb.00972
Cobb J. L., Santer R. M. Excitatory and inhibitory innervation of the heart of plaice (Pleuronectes platessa); anatomical and electrophysiological studies. Journal of Physiology, 1972, vol. 222, iss. suppl., pp. 42–43.
Gut P., Reischauer S., Stainier D. Y. R., Arnaut R. Little fish, big data: Zebrafish as a model for cardiovascular and metabolic disease. Physiological Reviews, 2017, vol. 97, no. 3, pp. 889–938. https://doi.org/10.1152/physrev.00038.2016
Harris M. B., Milsom W. K. Vagal feedback is essential for breathing in unanesthetized ground squirrels. Respiration Physiology, 2001, vol. 125, iss. 3, pp. 199–212. https://doi.org/10.1016/S0034-5687(00)00220-6
Jordan D., Spyer K. M. Central neural mechanisms mediating respiratory-cardiovascular interactions. In: Neurobiology of the Cardiorespiratory System. Manchester : Manchester University Press, 1987, pp. 322–341.
Kolesnikova E. E., Golovina I. V. Oxidoreductase activities in oxyphilic tissues of the Black Sea ruff Scorpaena porcus under short-term hydrogen sulfide loading. Journal of Evolutionary Biochemistry and Physiology, 2020, vol. 56, no. 5, pp. 459–470. https://doi.org/10.1134/S0022093020050099
Priede I. G. The effect of swimming activity and section of the vagus nerves on heart rate in rainbow trout. Journal of Experimental Biology, 1974, vol. 60, iss. 2, pp. 305–319. https://doi.org/10.1242/jeb.60.2.305
Saito T. Effects of vagal stimulation on the pacemaker action potentials of carp heart. Comparative Biochemistry and Physiology Part A: Physiology, 1973, vol. 44, iss. 1, pp. 191–199. https://doi.org/10.1016/0300-9629(73)90381-2
Satchell G. H. Respiratory reflexes in the dogfish. Journal of Experimental Biology, 1959, vol. 36, iss. 1, pp. 62–71. https://doi.org/10.1242/jeb.36.1.62
Soldatov A. A. Physiological aspects of effects of urethane anesthesia on the organism of marine fishes. Hydrobiological Journal, 2005, vol. 41, no. 1, pp. 113–126. https://doi.org/10.1615/HydrobJ.v41.i1.130
Soldatov A. A., Golovina I. V., Kolesnikova E. E., Sysoeva I. V., Sysoev A. A., Kukhareva T. A., Kladchenko E. S. Activity of energy metabolism enzymes and ATP content in the brain and gills of the Black Sea scorpionfish Scorpaena porcus under short-term hypoxia. Journal of Evolutionary Biochemistry and Physiology, 2020, vol. 56, iss. 3, pp. 224–234. https://doi.org/10.1134/S0022093020030059
Sun P., Zhang Y., Yu F., Parks E., Lyman A., Wu Q., Ai L., Hu C. H., Zhou Q., Shung K., Lien C. L., Hsiai T. K. Micro-electrocardiograms to study post-ventricular amputation of zebrafish heart. Annals of Biomedical Engineering, 2009, vol. 37, no. 5, pp. 890–901. https://doi.org/10.1007/s10439-009-9668-3
Sutterlin A. M., Saunders R. L. Proprioceptors in the gills of teleosts. Canadian Journal of Zoology, 1969, vol. 47, no. 6, pp. 1209–1212. https://doi.org/10.1139/z69-188
Taylor E. W. Nervous control of the heart and cardiorespiratory interactions. In: Fish Physiology. New York : Academic Press, 1992, pp. 343–387.
Taylor E. W., Jordan D., Coote J. H. Central control of the cardiovascular and respiratory systems and their interactions in vertebrates. Physiological Reviews, 1999, vol. 79, iss. 3, pp. 855–916. https://doi.org/10.1152/physrev.1999.79.3.855
Taylor E. W., Leite C. A. C., Levings J. J. Central control of cardiorespiratory interactions in fish. Acta Histochemica, 2009, vol. 111, iss. 3, pp. 257–267. https://doi.org/10.1016/j.acthis.2008.11.006
Taylor E. W., Leite C. A., Sartori M. R., Wang T., Abe A. S., Crossley D. A. The phylogeny and ontogeny of autonomic control of the heart and cardiorespiratory interactions in vertebrates. Journal of Experimental Biology, 2014, vol. 217, iss. 5, pp. 690–703. https://doi.org/10.1242/jeb.086199
Young M. J., Taylor E. W., Butler P. J. Central electrical stimulation of the respiratory nerves of the anaesthetized, decerebrate dogfish, Scyliorhinus, and its effect on fictive respiration. Journal of Physiology, 1993, vol. 459, iss. suppl., pp. 104.