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Effects of changes in inspired gas composition on ventilation and breathing pattern in awake and hibernating ground squirrels McArthur, M. Dawn


During entrance into hibernation in mammals, continuous breathing is converted to intermittent breathing in conjunction with the reductions in metabolic rate (MR) and body temperature (T[sub B]). The intermittent breathing pattern is characterized by long non-ventilatory periods (T[sub NVP]) , which are interrupted by bursts of several breaths (Cheyne-Stokes respiration, CSR) in some species, or by only single breaths in other species. The nature of this species difference in intermittent breathing pattern has remained a puzzle, due mainly to the problems of measuring ventilation accurately in undisturbed hibernating animals. In this study, I examined the ventilatory responses of two species of ground squirrel that display each of the two intermittent breathing patterns during hibernation. These experiments were designed to test the hypothesis that the species difference in intermittent breathing pattern can be explained on the basis of a difference in sensitivity to hypoxia and hypercapnia. When awake and euthermic at a T[sub A] of 22°C, both the golden-mantled ground squirrel (Spermophilus lateralis) and the Columbian ground squirrel (S. columbianus) breathe continuously. Ventilation and ventilatory responses were measured in awake animals using whole body plethysmography. In response to a decrease in the fractional inspired O₂ concentration (F[sub IO2]) below 15-10% both species increased ventilation mainly via an increase in breathing frequency (f); tidal volume (V[sub T]) was increased only when F[sub IO2]was lowered to 5%. When the fractional inspired CO₂ concentration (F[sub ICO2])was increased, both species responded by increasing f and V[sub T], so that minute ventilation increased linearly with F[sub ICO2]. In S. columbianus, these response patterns were unaffected by acute cold exposure. During periodic arousal from hibernation in the same species hypoxic responses remained the same, but hypercapnic responses appeared to be slightly elevated. Relative to non-fossorial, non-hibernating mammals, the two ground squirrel species showed comparable hypoxic responses, but blunted hypercapnic responses. These ventilatory responses are typical of burrowing animals, such as these ground squirrels. In hibernating animals, ventilation was measured using a face-mask and pneumotachograph. S. lateralis exhibited CSR, while S. columbianus showed only single breaths. Both species had similar overall levels of ventilation and continued to show similar ventilatory responses to hypoxic and hypercapnic gas mixtures. Due to the decreases in T[sub B] and MR and the increase in hemoglobin-O₂ affinity during hibernation, hypoxic sensitivity was negligible in both species. In contrast, hypercapnic responses, though reduced in absolute terms during hibernation, were in fact enhanced relative to resting MR. In both S. lateralis and S. columbianus, ventilation was increased during hypercapnic exposure solely by a decrease in T[sub NVP]. This suggests that there has been a shift in central integration of afferent information, since in contrast to euthermia, in hibernation the non-ventilatory period, not the breath, appears to be the major controlled variable of the breathing pattern. These patterns of ventilatory response to hypoxia and hypercapnia suggest that in euthermia changes in PO₂ play a predominant role in ventilatory control, whereas in hibernation ventilation is controlled by changes in PCO₂ or pH. This was found to be true for both species, despite the presence of two distinct intermittent breathing patterns. Thus the results do not support the hypothesis that this difference in breathing pattern during hibernation can be accounted for by a difference in sensitivity to respiratory gases. This study has shown that ventilatory control mechanisms are maintained in the deeply hibernating animal. Only hypoxic sensitivity is reduced during hibernation; hypercapnic sensitivity appears, in fact, to be augmented, presumably enabling the animal to effectively control its ventilation to meet the requirements for gas exchange and acid-base balance.

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