The hidden secrets of the hibernator’s heart may protect against arrhythmias

Abstract

In this issue of Heart Rhythm, Fedorov et al 1 describe the activation pattern and other electrophysiologic features of the heart of Citellus undulatus (also known as Spermophilus undulatus), the Siberian ground squirrel, both in summer active and in winter hibernating animals at temperatures varying from 3°C to 37°C and compared those with data in the rabbit heart as a nonhibernating species. The summary of the data can be simple. There is a substantial decrease in conduction velocity from 70 -80 cm/s in the Siberian ground squirrel at 37°C to 5-10 cm/s at 3°C. However, the conduction patterns remain normal and do not show areas of substantial conduction block, which might herald arrhythmias. Interestingly, conduction velocity was significantly higher in hearts obtained from winter hibernating animals than from summer active animals at both 37°C and 3°C. Data at such low temperatures cannot be obtained from the hearts in nonhibernating species such as the rabbit in the present study, but also not in man, because their hearts become quiescent or develop ventricular fibrillation at temperatures below 20°C. 1,2 Moreover, the authors show that there is an up-regulation of connexin43 (Cx43) in working ventricular myocardium of hibernating animals, in line with previous research, 3 and an appearance of connexin45 (Cx45) in working ventricular myocardium, although the expression of the latter normally is restricted to the conduction system. 4 This study underscores the presence of differences not only between hibernating and nonhibernating species but also between hibernating and nonhibernating individuals of the same species, with all the interesting implications for regulatory mechanisms. Physiologic background and implicationsWe would like to point out first that hypothermia impairs conduction velocity by a combined effect on the underlying membrane currents and on gap junctions. The conductance of gap junctions is reduced by about 70% when the temperature drops from normal to 0°C at least in cell pairs of neonatal rat heart. 5 Whether the inward Na ϩ current is operational at temperatures well below 10°C is questionable because it is seriously impaired at much smaller drops in temperature than those observed in hibernators. 6,7 Liu et al 8 reported that the L-type Ca 2ϩ current virtually disappears at 10°C in rat ventricular myocytes, although rat ventricle is relatively resistant against low temperature compared with other mammals. In contrast, the L-type Ca 2ϩ current has the same amplitude in hedgehog papillary muscle in the temperature range from 10°C to 35°C. 8 It is not possible to decide whether conduction remains intact, although impaired, in hibernators at temperatures well below 10°C because their membrane currents are relatively resistant against low temperature or because their gap junctions function better at low temperature compared with nonhibernators. Of note, in this study arrhythmias did not develop despite conduction velocities of 5 cm/s in the hearts from summer active animals at 3°C and conduc...

Cold-hearted bats: uncoupling of heart rate and metabolism during torpor at subzero temperatures

“…While temperate zone northern hemisphere bats tend to hibernate in thermally stable caves or mines during winter, many southern hemisphere bats hibernate in tree hollows or under bark. These roosts are thermally labile and often experience sub-zero T a (Law and Chidel, 2007;Turbill, 2008;Clement and Castleberry, 2013;Stawski and Currie, 2016). Information concerning cardiac function and its relationship to metabolism and thermal energetics in this species, or at such low temperatures in any bat, is entirely lacking.…”

Cardiac dynamics during daily torpor in the Djungarian hamster (Phodopus sungorus)

“…Generally, the terms "daily torpor" and "hibernation" are merely descriptive for the duration of the dormant state and may not be indicative of a difference in fundamental physiological mechanisms between the two categories. Several reviews provide comprehensive coverage of the physiological mechanisms of hibernation and torpor (5,7,14,19,21,25,26,29,36,41).Remarkably, the Djungarian or Siberian hamster (Phodopus sungorus), which inhabits regions of southwestern Siberia and northeastern Kazakhstan, is not a deep hibernator, although it opportunistically may undergo periods of daily torpor for 5-10 h with T b as low as 15°C (37). In this species, the expression of daily torpor is part of seasonal acclimation triggered by short photoperiods and involves an array of morphological and physiological adaptations, including weight loss, appearance of winter pelage, reproductive quiescence, and increased capacity for nonshivering thermogenesis.…”

“…Generally, the terms "daily torpor" and "hibernation" are merely descriptive for the duration of the dormant state and may not be indicative of a difference in fundamental physiological mechanisms between the two categories. Several reviews provide comprehensive coverage of the physiological mechanisms of hibernation and torpor (5,7,14,19,21,25,26,29,36,41).…”