Is cold acclimation of benefit to hibernating rodents?

Abstract

Summary The thermal challenge associated with cold acclimation (CA) and hibernation requires effective cardio-respiratory function over a large range of temperatures. We examined the impact of acute cooling in a cold-naive hibernator to quantify the presumed improvement in cardio-respiratory dysfunction triggered by CA, and estimate the role of the autonomic nervous system in optimising cardiac and respiratory function. Golden hamsters (Mesocricetus auratus) were held at a 12h:12h light/dark (L:D) photoperiod and room temperature (21°C euthermic control) or exposed to simulated onset of winter in an environmental chamber, by progression to 1h:23h L:D and 4°C over 4weeks. In vivo acute cooling (core temperature Tb=25°C) in euthermic controls led to a hypotension (P<0.05), bradycardia (P<0.05) but preserved cardiac output (NS). CA induced a hypertension at normothermia (Tb=37°C) but on cooling led to decreases in diastolic pressure below euthermic controls (P<0.05) and a decrease in cardiac output (P<0.05), despite an increase in left ventricular conductance (P<0.05). Power Spectral Analysis of heart rate variability suggested a decline in vagal tone on cooling euthermic hamsters (P<0.05 at Tb=25°C). Following CA, vagal tone was increased at Tb=37°C (P<0.05), but declined more quickly on cooling (Tb=25°C) to preserve vagal tone at levels similar to euthermic controls at Tb=37°C. For the isolated heart, CA led to concentric hypertrophy (P<0.05) with decreased end-diastolic volume (P<0.05) but with no change in intrinsic heart rate at either T=37°C or T=25°C (NS). Mechanical impairment was noted at T=37°C following CA, with peak developed pressure decreased by 50% (P<0.05) and peak rate-pressure product decreased by 65% (P<0.05); this difference was preserved at T=25°C. For euthermic hearts, coronary flow showed thermal sensitivity, decreasing 65% on cooling (T=25°C; P<0.05). By contrast, CA hearts had low coronary flow (P<0.05 compared to euthermic control) but with a loss of thermal sensitivity (NS). Together, these observations suggest that CA induced a functional impairment in the myocardium that limits performance of the cardiovascular system at euthermia, despite increased autonomic input to preserve cardiac function. On acute cooling this autonomic control was lost and cardiac performance declined further than for cold-naive hamsters, suggesting CA may compromise elements of cardiovascular function to facilitate preservation of those more critical for subsequent rewarming.