Abstract
Previous reports suggested the existence of direct somatic motor control over heart rate (fH) responses during diving in some marine mammals, as the result of a cognitive and/or learning process rather than being a reflexive response. This would be beneficial for O2 storage management, but would also allow ventilation-perfusion matching for selective gas exchange, where O2 and CO2 can be exchanged with minimal exchange of N2. Such a mechanism explains how air breathing marine vertebrates avoid diving related gas bubble formation during repeated dives, and how stress could interrupt this mechanism and cause excessive N2 exchange. To investigate the conditioned response, we measured the fH-response before and during static breath-holds in three bottlenose dolphins (Tursiops truncatus) when shown a visual symbol to perform either a long (LONG) or short (SHORT) breath-hold, or during a spontaneous breath-hold without a symbol (NS). The average fH (ifHstart), and the rate of change in fH (difH/dt) during the first 20 s of the breath-hold differed between breath-hold types. In addition, the minimum instantaneous fH (ifHmin), and the average instantaneous fH during the last 10 s (ifHend) also differed between breath-hold types. The difH/dt was greater, and the ifHstart, ifHmin, and ifHend were lower during a LONG as compared with either a SHORT, or an NS breath-hold (P < 0.05). Even though the NS breath-hold dives were longer in duration as compared with SHORT breath-hold dives, the difH/dt was greater and the ifHstart, ifHmin, and ifHend were lower during the latter (P < 0.05). In addition, when the dolphin determined the breath-hold duration (NS), the fH was more variable within and between individuals and trials, suggesting a conditioned capacity to adjust the fH-response. These results suggest that dolphins have the capacity to selectively alter the fH-response during diving and provide evidence for significant cardiovascular plasticity in dolphins.
Highlights
In 1870, Paul Bert published his work showing a remarkable bradycardia associated with apnea in ducks from 100 beats · min−1 while breathing at the surface to 14 beats · min−1 while submerged (Bert, 1870)
Irving proposed that the cardiovascular changes, with a diving bradycardia and peripheral vasoconstriction, result in decreased cardiac output (CO) that would conserve the available O2 for hypoxia sensitive tissues such as brain and heart (Irving, 1939)
We showed that anticipation of a LONG breathhold caused a faster reduction in f H to a lower average, and minimum f H during the first 20 s of the breath-hold than anticipation of a SHORT breath-hold
Summary
In 1870, Paul Bert published his work showing a remarkable bradycardia associated with apnea in ducks from 100 beats · min−1 while breathing at the surface to 14 beats · min−1 while submerged (Bert, 1870). Development of electronic devices that could record physiological changes continuously allowed the cardiovascular responses to be measured in freely diving birds and mammals These studies confirmed that a diving bradycardia was observed during voluntary dives, but it was much more variable and not always as extreme as during forced dives (Elsner, 1965, 1966; Elsner et al, 1966; Kooyman and Campbell, 1972; Jones et al, 1973; Butler and Woakes, 1979; Kanwisher et al, 1981; Blix and Kjekshus, 1983; Blix, 1987; Ponganis et al, 1991; Thompson and Fedak, 1993; Andrews et al, 1997; Ponganis et al, 1997; Houser et al, 2010; Fahlman et al, 2019b). Without a comparison of the reaction to trained symbols for different dive durations, conditioned control cannot be ascertained
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