Four-week cold acclimation in adult humans shifts uncoupling thermogenesis from skeletal muscles to BAT

Abstract

We previously showed that four weeks of daily cold exposure, in humans, can increase brown adipose tissue (BAT) volume by 45% and oxidative metabolism by 182%. Surprisingly, we did not find a reciprocal reduction in shivering intensity when exposed to a mild cold (18°C). The aim of the present study was to determine whether changes in skeletal muscle oxidative metabolism or shivering activity could account for these unexpected findings. Nine men participated in a four-week cold acclimation intervention (10°C water circulating in liquid-conditioned suit, 2 h/day, 5 days/week). Shivering intensity and pattern were measured continuously during a controlled cold exposure (150 min at 4°C) before and after the acclimation. Muscle biopsies from m. vastus lateralis were obtained to measure oxygen consumption rate and proton leak of permeabilized muscle fibers. Cold acclimation elicited a modest 21% (P < 0.05) decrease in whole-body and m.vastus lateralis shivering intensity. Further, cold acclimation abolished the acute cold-induced increase in proton leak. Although daily cold exposure did not change the fiber composition of the m. vastus lateralis, fiber composition was a strong predictor of the shivering pattern evoked during an acute cold. We conclude that muscle-derived thermogenesis during acute cold exposure in humans is not limited to shivering, but also includes cold-induced increases in proton leak. The efficiency of muscle oxidative phosphorylation improves with cold acclimation, suggesting that reduced muscle thermogenesis occurs through decreased proton leak, in addition to decreased shivering intensity as BAT capacity and activity increases. These changes occur with no net difference in whole-body thermogenesis.

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