Relative enlargement of the medial preoptic nucleus in the Etruscan shrew, the smallest torpid mammal

Abstract

Endothermy is a key feature of mammalian biology and enables mammals to maintain stable body temperature and homeostatic functions in the face of a rapidly changing environment. However, when faced with harsh environmental conditions, certain mammalian species enter torpor, a state characterized by reduced metabolism, body temperature, and activity, to minimize energy loss. Etruscan shrews are the smallest mammals, with a surface-to-volume ratio that is very unfavorable for endothermic animals. As a result, Etruscan shrews have an extremely high metabolic rate and are known to enter torpor frequently, presumably as an energy-saving measure. Despite the recent identification of medial preoptic area (MPA) as a key brain region to regulate torpor in mouse, little is known about neural control of torpor in other endothermic animals, including the Etruscan shrew. Here, we confirmed that Etruscan shrews readily enter torpor even in the absence of strong physiological triggers. We then compared the medial preoptic nucleus (MPN) within the MPA of Etruscan shrew and rat, a mammal that does not enter torpor under physiological conditions. While rats have roughly 100 times the body weight and 33 times the brain weight of Etruscan shrews, we find that the male rat MPN exhibits only 6.7 times the volume of that of the male Etruscan shrew. Accordingly, the relative brain volume of the MPN was 6.5-fold larger in shrews, a highly significant difference. Moreover, MPN neuron counts were only roughly twofold lower in shrews than in rats, an astonishing observation considering the interspecies size difference and that neocortical neurons are ~ 20 × more numerous in rats than in shrews. We suggest that the extraordinary enlargement of the Etruscan shrew MPN is a specialization for orchestrating torpor in a mammal with an exceptional metabolism.