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Effects of low temperature on breathing pattern and ventilatory responses during hibernation in the golden-mantled ground squirrel

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Abstract

During entrance into hibernation in golden-mantled ground squirrels (Callospermophilus lateralis), ventilation decreases as metabolic rate and body temperature fall. Two patterns of respiration occur during deep hibernation. At 7 °C body temperature (T b ), a breathing pattern characterized by episodes of multiple breaths (20.6 ± 1.9 breaths/episode) separated by long apneas or nonventilatory periods (T nvp ) (mean = 11.1 ± 1.2 min) occurs, while at 4 °C T b , a pattern in which breaths are evenly distributed and separated by a relatively short T nvp (0.5 ± 0.05 min) occurs. Squirrels exhibiting each pattern have similar metabolic rates and levels of total ventilation (0.2 and 0.23 ml O2/hr/kg and 0.11 and 0.16 ml air/min/kg, respectively). Squirrels at 7 °C T b exhibit a significant hypoxic ventilatory response, while squirrels at 4 °C T b do not respond to hypoxia at any level of O2 tested. Squirrels at both temperatures exhibit a significant hypercapnic ventilatory response, but the response is significantly reduced in the 4 °C T b squirrels. Carotid body denervation has little effect on the breathing patterns or on the hypercapnic ventilatory responses. It does reduce the magnitude and threshold for the hypoxic ventilatory response. Taken together the data suggest that (1) the fundamental rhythm generator remains functional at low temperatures; (2) the hypercapnic ventilatory response arises from central chemoreceptors that remain functional at very low temperatures; (3) the hypoxic ventilatory response arises from both carotid body and aortic chemoreceptors that are silenced at lower temperatures; and (4) there is a strong correlation between breathing pattern and chemosensitivity.

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References

  • Barnes BM, Buck L (2000) Hibernation in the extreme: Burrow and body temperatures, metabolism, and limits to torpor bout length in Arctic ground squirrels. In: Heldmaier G, Klingenspor M. (eds) Life in the Cold. Springer, Heidelberg, pp 65–72

    Chapter  Google Scholar 

  • Biörck G, Johansson B, Schmidt H (1956) Reactions of hedgehogs, hibernating and non-hibernating to the inhalation of oxygen, carbon dioxide and nitrogen. Acta Physiol Scand 37:71–83

    Article  PubMed  Google Scholar 

  • Champagnat J, Fortin G (1997) Primordial respiratory-like rhythm generation in the vertebrate embryo. TINS 20:119–124

    CAS  PubMed  Google Scholar 

  • Cherniack NS, Longobardo GS (1981) The chemical control of respiration. Annal Biomed Eng 9:395–407

    Article  CAS  Google Scholar 

  • Cherniack NS, Longobardo G, Evangelista CJ (2005) Causes of Cheyne–Stokes respiration. Neurocrit Care 3:271–279

    Article  CAS  PubMed  Google Scholar 

  • Endres G, Taylor H (1930) Observations on certain physiological processes of the marmot. II. The respiration. Proc Roy Soc Lond Ser B 107:230–240

    Google Scholar 

  • Fong AY, Zimmer MB, Milsom WK (2009) The conditional nature of the “central rhythm generator” and the production of episodic breathing. Respir Physiol Neurobiol 168:179–187

    Article  PubMed  Google Scholar 

  • Gargaglioni LH, Meier JT, Branco LG, Milsom WK (2007) Role of midbrain in the control of breathing in anuran amphibians. Am J Physiol Regul Integr Comp Physiol 293:R447–R457

    Article  CAS  PubMed  Google Scholar 

  • Garland RJ, Kinkead R, Milsom WK (1994) The stimulus modality of the hypoxic ventilatory response in rodents. In: O’Regan R (ed) Arterial Chemoreceptors: cell to system. Plenum Press, New York, pp 369–371

    Chapter  Google Scholar 

  • Guyenet PG, Stornetta RL, Bayliss DA (2010a) Central respiratory chemoreception. J Comp Neurol 518:3883–3906

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guyenet PG, Stornetta RL, Abbott SB, Depuy SD, Fortuna MG, Kanbar R (2010b) Central CO2 chemoreception and integrated neural mechanisms of cardiovascular and respiratory control. J Appl Physiol 108:995–1002

    Article  PubMed  PubMed Central  Google Scholar 

  • Hammel HT, Dawson TJ, Abrams RM, Andersen HT (1968) Total calorimetric measurements on Citellus lateralis in hibernation. Physiol Zool 41:341–357

    Article  Google Scholar 

  • Khoo MCR, Kronauer KE, Strohl KP, Slutsky AS (1982) Factors producing periodic breathing in humans: a general model. J Appl Physiol 53:644–659

    CAS  PubMed  Google Scholar 

  • Kristoffersson R, Soivio A (1964) Hibernation in the hedgehog Erinaceus europaeus. Changes of respiratory pattern, heart rate and body temperature in response to gradually decreasing or increasing ambient temperature. Ann Acad Sci Fenn Ser A 482:3–17

    Google Scholar 

  • Kristoffersson R, Soivio A (1966) Duration of hypothermia periods and typeof respiration in the hibernating golden hamster, Mesocricetus auratus Waterh. Ann Zool Fenn 3:66–67

    Google Scholar 

  • Lahiri S, Maret K, Sherpa MG (1983) Dependence of high altitude sleep apnea on ventilator sensitivity to hypoxia. Respir Physiol 52:281–301

    Article  CAS  PubMed  Google Scholar 

  • Landau BR, Dawe AR (1958) Respiration in the hibernation of the 13-lined ground squirrel. Am J Physiol 194:75–82

    CAS  PubMed  Google Scholar 

  • Lyman CP, Hastings AB (1951) Total CO2 of hamsters and ground squirrels during hibernation. Am J Physiol 167:633–637

    CAS  PubMed  Google Scholar 

  • Lyman CP, Willis JS, Malan A, Wang LCH (1982) Hibernation and Torpor in mammals and birds. Academic Press, New York

    Google Scholar 

  • Maginniss LA, Milsom WK (1994) Effects of hibernation on blood oxygen transport in the golden mantled ground squirrel. Respir Physiol 95:195–208

    Article  CAS  PubMed  Google Scholar 

  • Malan A (1973) Ventilation measured by body plethysmography in hibernating mammals and poikilotherms. Respir Physiol 17:32–44

    Article  CAS  PubMed  Google Scholar 

  • Malan A (1982) Respiration and acid-base state in hibernation. In: Lyman CP, Willis JS, Malan A, Wang LCH (eds) Hibernation and torpor in Mammals and birds. Academic Press, New York

    Google Scholar 

  • Malan A, Arens H, Waechter A (1973) Pulmonary respiration and acid–base state in hibernating marmots and hamsters. Respir Physiol 17:45–61

    Article  CAS  PubMed  Google Scholar 

  • McArthur MD, Milsom WK (1991) Changes in ventilation and respiratory sensitivity associated with hibernation in Columbian (Spermophilus columbianus) and Golden-mantled (Spermophilus lateralis) ground squirrels. Physiol Zool 64:940–959

    Article  Google Scholar 

  • Milsom WK, Jackson DC (2011) Hibernation and gas exchange. Comprehensive. Physiology 1:397–420

    Google Scholar 

  • Naifeh KH, Huggins SE, Hoff HE (1971) Effects of brain section on respiratory patterns of crocodilian reptiles. Respir Physiol 13:186–197

    Article  CAS  PubMed  Google Scholar 

  • Nattie E, Li A (2012) Central chemoreceptors: locations and functions. Comprehensive. Physiology 2:221–254

    Google Scholar 

  • Pajunen I (1970) Body temperature, heart rate, breathing pattern, weight loss and periodicity of hibernation in the Finnish garden dormouse Eliomys quercinus L. Ann Zool Fenn 7:251–266

    Google Scholar 

  • Pajunen I (1984) Ambient temperature dependence of the periodic respiratory pattern during long-term hibernation in the garden dormouse, Eliomys quercinus L. Ann Zool Fenn 21:143–148

    Google Scholar 

  • Pembry MS, Pitts AG (1899) The relationship between the internal temperature and the respiratory movements of hibernating animals. J Physiol 24:305–316

    Article  Google Scholar 

  • Reid SG, Milsom WK (1998) Respiratory pattern formation in the isolated bullfrog (Rana catesbeiana) brainstem-spinal cord. Respir Physiol 114:239–255

    Article  CAS  PubMed  Google Scholar 

  • Reid SG, Meier JT, Milsom WK (2000) The influence of descending inputs on breathing pattern formation in the isolated bullfrog brainstem-spinal cord. Respir Physiol 120:197–211

    Article  CAS  PubMed  Google Scholar 

  • Steffen JM, Reidesel ML (1982) Pulmonary ventilation and cardiac activity in hibernating and arousing golden-mantled ground squirrels (Spermophilus lateralis). Cryobiology 19:83–91

    Article  CAS  PubMed  Google Scholar 

  • Tahti H (1975) Effects of changes in CO2 and O2 concentrations in the inspired gas on respiration in the hibernating hedgehog (Erinaceus europaeus L.). Ann Zool Fenn 12:183–187

    CAS  Google Scholar 

  • Tahti HM, Nikinmaa M, Soivio A (1981) Cheyne Stokes breathing pattern as an adaptation to deep hibernation hypothermia. Cryobiology 18:92

    Article  Google Scholar 

  • Webb CL, Milsom WK (1990) Carotid body contribution to hypoxic ventilator responses in euthermic and hibernating ground squirrels. In: Eyzaguirre C, Fidone SJ, Fitzgerald RS, Lahiri S, McDonald DM (eds) Arterial chemoreception. Springer, New York, pp 337–343

    Chapter  Google Scholar 

  • Webb CL, Milsom WK (1994) Ventilatory responses to acute and chronic hypoxic hypercapnia in the ground squirrel. Respir Physiol 98:137–152

    Article  CAS  PubMed  Google Scholar 

  • Yumino D, Bradley TD (2008) Central sleep apnea and Cheyne–Stokes respiration. Proc Am Thoracic Soc 5:226–236

    Article  Google Scholar 

  • Zimmer MB, Milsom WK (2001) Effects of changing ambient temperature on metabolic, heart, and ventilation rates during steady state hibernation in golden-mantled ground squirrels (Spermophilus lateralis). Physiol Biochem Zool 74:714–723

    Article  CAS  PubMed  Google Scholar 

  • Zimmer MB, Milsom WK (2004) Effect of hypothermia on respiratory rhythm generation in hamster brainstem-spinal cord preparations. Resp Physiol Neurobiol 142:237–249

    Article  Google Scholar 

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Funding

This research was funded by the NSERC of Canada.

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Correspondence to William K. Milsom.

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Communicated by F. Breukelen.

This manuscript is part of the special issue Hibernation—Guest Editors: Frank van Breukelen and Jenifer C. Utz.

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Webb, C.L., Milsom, W.K. Effects of low temperature on breathing pattern and ventilatory responses during hibernation in the golden-mantled ground squirrel. J Comp Physiol B 187, 793–802 (2017). https://doi.org/10.1007/s00360-017-1079-4

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  • DOI: https://doi.org/10.1007/s00360-017-1079-4

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