Naked mole rats exhibit metabolic but not ventilatory plasticity following chronic sustained hypoxia

Abstract

ResearchCite this article: Chung D, Dzal YA, Seow A, Milsom WK, Pamenter ME. 2016 Naked mole rats exhibit metabolic but not ventilatory plasticity following chronic sustained hypoxia. Naked mole rats are among the most hypoxia-tolerant mammals identified and live in chronic hypoxia throughout their lives. The physiological mechanisms underlying this tolerance, however, are poorly understood. Most vertebrates hyperventilate in acute hypoxia and exhibit an enhanced hyperventilation following acclimatization to chronic sustained hypoxia (CSH). Conversely, naked mole rats do not hyperventilate in acute hypoxia and their response to CSH has not been examined. In this study, we explored mechanisms of plasticity in the control of the hypoxic ventilatory response (HVR) and hypoxic metabolic response (HMR) of freely behaving naked mole rats following 8-10 days of chronic sustained normoxia (CSN) or CSH. Specifically, we investigated the role of the major inhibitory neurotransmitter g-amino butyric acid (GABA) in mediating these responses. Our study yielded three important findings. First, naked mole rats did not exhibit ventilatory plasticity following CSH, which is unique among adult animals studied to date. Second, GABA receptor (GABAR) antagonism altered breathing patterns in CSN and CSH animals and modulated the acute HVR in CSN animals. Third, naked mole rats exhibited GABAR-dependent metabolic plasticity following longterm hypoxia, such that the basal metabolic rate was approximately 25% higher in normoxic CSH animals than CSN animals, and GABAR antagonists modulated this increase.

The hypoxia tolerance of eight related African mole‐rat species rivals that of naked mole‐rats, despite divergent ventilatory and metabolic strategies in severe hypoxia

“…However, ventilation accounts for only part of the hypoxic response as many semi‐fossorial and fossorial species employ a strategy that also includes decreases in metabolism . NMRs combat low environmental O 2 with a large reduction in aerobic metabolism, thus matching O 2 demand to a depleted O 2 supply . The mole‐rat species reported in this study, with the exception of G.c.…”

“…Previous work has shown that the NMR is among the most hypoxia‐tolerant mammals, responding to extreme hypoxia with no change in ventilation and large reductions in metabolism (Figure ). This is hypothesized to be the result of an evolutionary pressure exerted by low oxygen availability resulting from their fully fossorial and eusocial lifestyle, which could possibly be facilitated by a retention of neonatal traits .…”

“…has a ventilatory response that surpasses those of most other species. NMRs, on the other hand, exhibit little or no ventilatory response to hypoxia …”

“…NMRs, on the other hand, exhibit little or no ventilatory response to hypoxia. 19,20 However, ventilation accounts for only part of the hypoxic response as many semi-fossorial and fossorial species employ a strategy that also includes decreases in metabolism. 15 NMRs combat low environmental O 2 with a large reduction in aerobic metabolism, thus matching O 2 demand to a depleted O 2 supply.…”

Brain atlas of the African mole‐ratFukomys anselli

“…Figure ). Physiologically, these animals show a high tolerance to hypoxic and hypercapnic conditions (Chung, Dzal, Seow, Milsom, & Pamenter, ; Larson & Park, ; Nevo, ; Park et al, ). Their sensory organs have also adapted to the dark and featureless underground environment (Burda, Bruns, & Müller, ).…”