Effects of age on thermoregulatory responses during cold exposure in a nonhuman primate, Microcebus murinus

Abstract

Cold resistance appears altered with aging. Among existing hypotheses, the impaired capacity in response to cold could be related to an altered regulation of plasma IGF-1 concentration. The combined effects of age and cold exposure were studied in a short-living primate, the gray mouse lemur (Microcebus murinus), which adjusts its energy balance using a daily torpor phase, to avoid high energy cost of normothermia maintenance. Changes in body mass, core temperature, locomotor activity, and caloric intake were monitored under 9-day exposures to 25 degrees C and 12 degrees C in captive animals in winter conditions. Short-term (after 2 days) and long-term (after 9 days) cold-induced changes in IGF-1 levels were also evaluated. In thermoneutral conditions (25 degrees C), general characteristics of the daily rhythm of core temperature were preserved with age. At 12 degrees C, age-related changes were mainly characterized by a deeper hypothermia and an increased frequency of torpor phases, associated with a loss of body mass. A short-term cold-induced decrease in plasma IGF-1 levels was observed. IGF-1 levels returned to basal values after 9 days of cold exposure. No significant effect of age could be evidenced on IGF-1 response. However, IGF-1 levels of cold-exposed aged animals were negatively correlated with the frequency of daily torpor. Responses exhibited by aged mouse lemurs exposed to cold revealed difficulties in the maintenance of normothermia and energy balance and might involve modulations of IGF-1 levels.

Impaired Control of Body Cooling during Heterothermia Represents the Major Energetic Constraint in an Aging Non-Human Primate Exposed to Cold

“…In fact, shallow daily heterothermia is widely used in small mammal species for limiting the energy costs of normothermia [for review], [see 2,3]. Also, this privileged mechanism of energy and water savings is particularly enhanced during winter in the mouse lemur, such as it has already been evidenced in captive conditions [7]. In fact, during winter, season corresponding to food and water scarcity, mouse lemurs lower their metabolic rate and rest, leading thus to increased body mass.…”

“…More, Insulin-like Growth Factor type 1 (IGF-1) has been proposed to act in cold-induced thermogenesis processes in the rat [40], [41]. It appeared that IGF-1 levels were higher during summer [23] than during winter [7], what could also contribute to the seasonal difference in heterothermia depth.…”

“…However, it is likely that the trade-off between the energy saved during daily heterothermia and the energetic cost of arousal impacts energy balance. In this manner, we recently observed from core temperature (Tc) recording and body mass changes indirect evidences that aging may significantly affect such trade-off during cold-induced energy stress in the gray mouse lemur [7]. Indeed, the loss of body mass during cold exposure despite higher expression of daily heterothermia observed in aged, but not adult gray mouse lemurs, suggests that deep daily heterothermia episodes in aged heterotherms increase rather than decrease daily energy expenditure [8], [9].…”

“…The underlying hypothesis is that deep daily heterothermia expression in aged animals is an energy costly, but obligatory process due to poor body insulation, as compared to the well described energy saving advantages in adults [5], [6]. As daily heterothermia appeared affected during cold exposure in aged animals acclimated to winter [7] but not in those acclimated to summer [23], we further tested the hypothesis that the impact of cold-induced stress on the energy budget will differ according to season.…”

“…These mechanisms are particularly enhanced during winter, a season during which water and food are scarce and Ta can reach very low values. In captive gray mouse lemurs, there are many evidences of strong interactions between the daily rhythm of Tc and photoperiod [16], ambient temperatures [7], [14], [16] and food availability [14], [17], suggesting that modulation of Tc is a key adaptive mechanism in this species. Finally, the mean life span of the mouse lemur in captivity is about 8 years [18], and aging is associated in this primate with a decrease in amplitude of the seasonal variations in body mass, gonadal hormones [19], melatonin [20], and DHEA-S [21], [22].…”