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When the brain goes diving: Adaptations for cerebral hypoxia tolerance in diving mammals

Lars P. Folkow1*
  • 1 University of Tromsø, Department of Arctic and Marine Biology, Norway

Aquatic mammals that forage at depth must endure extended breath-hold dives that for some species may last for two hours. With no access to oxygen other than that carried in their body, their diving performance depends heavily on elevated tissue levels of hemoglobin and myoglobin which give some species an oxygen-storing capacity that is almost 4 times as high as in non-specialist divers, like man. Further, profound cardiovascular adjustments may cause a redistribution of a much reduced cardiac output, in benefit of hypoxia-sensitive organs like the brain but at the expense of most other tissues, thus assuring that the oxygen is utilized at a much reduced pace. Still, their diving behavior often leaves these animals in a state of severe hypoxemia, with arterial oxygen tension (PaO2) regularly dropping below 20 mmHg in some species (Meir et al., 2009). At such critically low PaO2 levels, most mammals are at high risk of losing consciousness but diving species appear to suffer no ill-effects, implying an unusually high cerebral hypoxia tolerance. A diving-induced, vascularly mediated body cooling may contribute to this end by causing brain temperature to drop by up to 3 degrees Celsius, thereby presumably depressing metabolism as well as offering protection against hypoxic and oxidative stresses (Blix et al., 2010). Studies of metabolic adaptations moreover show that their brain tissue typically has elevated levels of glycogen and a high anaerobic capacity. Less is known about adaptive mechanisms at the cellular level, which in part is related to the inherent difficulties in obtaining neurophysiological data from these mammals, but some new information has recently emerged. Thus, in vitro studies using brain slices from hooded seals, Cystophora cristata, have shown that seal neurons have intrinsic properties that allow them to survive under severely hypoxic conditions (Folkow et al., 2008). Recent studies also suggest that the neurally based oxygen-binding protein neuroglobin (Ngb), a globin distantly related to hemoglobin and myoglobin, is involved in conferring hypoxia tolerance to the diving brain: In those non-diving species that have been studied, Ngb is predominantly expressed in neurons, while seals display the highest levels of Ngb in their glia cells (astrocytes). Since Ngb is typically associated with mitochondria and evidently supports oxidative metabolism, this difference implies an unusual metabolic organization in the seal brain that may enhance hypoxia tolerance (Mitz et al., 2009). In vitro studies also suggest that hypoxia-induced shut-down mechanisms that may involve inhibitory synaptic activity and channel arrest, cause neuronal hypometabolism and thereby enhanced hypoxic survival.

References

Blix, A.S., Walløe, L., Messelt, E.B., and Folkow, L.P. (2010). Selective brain cooling and its vascular basis in diving seals. J. Exp. Biol. 213, 2610-2616.
Folkow, L.P., Ramirez, J.-M., Ludvigsen, S., Ramirez, N., and Blix, A.S. (2008). Remarkable neuronal hypoxia tolerance in the deep-diving adult hooded seal (Cystophora cristata). Neurosci. Lett. 446, 147-150.
Meir, J.U., Champagne, C.D., Costa, D.P., Williams, C.L., and Ponganis, P.J. (2009).
Extreme hypoxemic tolerance and blood oxygen depletion in diving elephant seals. Am. J. Physiol. Regul. Integr. Comp. Physiol. 297, R927-R939.
Mitz, S.A., Reuss, S., Folkow, L.P., Blix, A.S., Ramirez, J.-M., Hankeln, T., and Burmester, T. (2009). When the brain goes diving: glial oxidative metabolism may confer hypoxia tolerance to the seal brain. Neurosci. 163, 552-560.

Keywords: Brain, Diving, hypometabolism, hypoxia, Neuroglobin, Seals

Conference: Tenth International Congress of Neuroethology, College Park. Maryland USA, United States, 5 Aug - 10 Aug, 2012.

Presentation Type: Invited Symposium (only for people who have been invited to a particular symposium)

Topic: Evolution

Citation: Folkow LP (2012). When the brain goes diving: Adaptations for cerebral hypoxia tolerance in diving mammals. Conference Abstract: Tenth International Congress of Neuroethology. doi: 10.3389/conf.fnbeh.2012.27.00040

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Received: 30 Apr 2012; Published Online: 07 Jul 2012.

* Correspondence: Prof. Lars P Folkow, University of Tromsø, Department of Arctic and Marine Biology, Tromsø, NO-9037, Norway, lars.folkow@uit.no