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Control of apnea in the hibernating ground squirrel

University of British Columbia

During hibernation the breathing pattern of the golden-mantled ground squirrel consists of short episodes of breathing separated by pauses ranging in length from less than a minute to greater than 30 minutes. A breathing pattern as such results in wide fluctuations in the partial pres sure of oxygen (PO₂ )and carbon dioxide (PCO₂)in the blood and lungs; the increase in PO₂ and decrease in PCO₂ during a breathing episode are reversed in the following apnea. These oscillations raise questions about the mechanisms involved in the initiation and termination of breathing episodes. Accompanying the profound reduction in ventilation is an alteration in the relative sensitivities to hypercapnia and hypoxia. While the ventilatory response to hypercapnia is elevated during hibernation compared to euthermia, the hypoxic ventilatory response (HYR) appears blunted, suggesting that changes in O₂ have little or no role in the control of episodic breathing. Despite an absolute reduction in the arterial oxygen partial pressure (PaO₂) threshold of the HVR, however, a strong correlation between the P2ao values for the threshold of the HVR and the shoulder of the oxyhemoglobin equilibrium curve (OEC) persists in heterothermic rodents as body temperature changes. It has been suggested that this may reflect either temperature induced changes in the response characteristics of arterial chemoreceptors or an ability to sense changes in arterial oxygen content (CaoO₂). Thus, the first series of experiments in this thesis examined the extent to which changing CaO₂ independent of PaO₂ with carbon monoxide hypoxia could contribute to the HVR in heterothermic (golden-mantled ground squirrels) and nonheterothermic (rats) rodents. The HVR of isocapnic, anaesthetized rodents was assessed during both hypoxic hypoxia, which alters PaO₂ and CaO₂ simultaneously, and carbon monoxide hypoxia, which alters CaO₂ independent of PaO₂ While both species exhibited ventilatory responses to hypoxic hypoxia and carbon monoxide hypoxia, the HVR of the squirrel was consistently higher than that of the rat. Reductions in C2ao independent of P2ao could produce only 60% of the full HVR seen with hypoxic hypoxia in both species. Simultaneous changes in PaO₂ were necessary to produce the full response. While it seems likely that the results can be explained by the changes in the tissue PO₂ which would occur at receptor sites under various conditions, such an explanation is not totally supported by other studies. So, although the HVR in hibernating animals is blunted, the golden-mantled ground squirrel can respond to changes in CaO₂ independent of PaO₂ and thus, changes in O₂ accompanying the ventilation-apnea cycle cannot be dismissed as playing a role in the control and genesis of episodic breathing. The second series of experiments in this thesis examined the possible role of fluctuations in O₂ and CO₂ levels over the ventilation-apnea cycle in initiating or terminating breathing episodes. Computerized tomography scans of two hibernating animals indicated that the glottis was closed and that apneic oxygenation could not occur. Analysis of end-tidal gas composition, indicative of arterial blood gas composition, revealed no clear cut thresholds in gas composition for initiating or terminating episodes of breathing. Over the course of the breathing episode, however, O₂ consumption fell exponentially while CO₂ production fell in a linear fashion. The breathing episode terminated at the point where O₂ consumption asymptoted suggesting that the length of the episode was just sufficient to repay the O₂ debt which accumulated during the preceding period of apnea. The oxidative costs associated with breathing episodes in these animals was calculated to be approximately 90% of the total metabolic rate during hibernation. This suggests that the metabolic rate is not constant during hibernation but varies in a cyclic fashion associated with the breathing pattern. It further suggests that although blood gas levels play a key role in establishing the total level of ventilation, the cyclic variations in their composition , associated with periods of apnea and eupnea, do not by themselves initiate or terminate breathing episodes.

Thesis/Dissertation

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2009-02-23

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http://hdl.handle.net/2429/4950

Zoology

University of British Columbia

UBCV

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