Journal of Comparative Physiology B

, Volume 189, Issue 6, pp 685–692 | Cite as

A robust diving response in the laboratory mouse

  • Elissa M. Hult
  • Mark J. Bingaman
  • Steven J. SwoapEmail author
Original Paper


The diving response is a coordinated physiological response to submersion under water and has been documented amongst all mammals tested to date. The physiological response consists of three primary reflexes: an immediate bradycardia, apnea, and selective constriction of peripheral blood vessels. We hypothesized that mice would exhibit a diving response upon voluntary submersion into water typically seen in other mammals. In this study, telemeters that measure arterial pressure were implanted into male and female C57Bl/6J mice. These mice were trained to voluntarily dive underwater for a distance of 40 cm over a 4–6 s period. Just before the dive, the interbeat interval (IBI) was 87 ± 6 ms (mean ± SD) and diastolic pressure was 99 ± 14 mmHg. Underwater submersion caused (1) a dramatic bradycardia immediately at the onset of each dive, as IBI increased to 458 ± 104 ms, and (2) a large drop in diastolic pressure, to 56 ± 16 mmHg despite the elevation in peripheral resistance. Mice experienced a short bout (~ 2 s) of hypertension (diastolic pressure rose to 131 ± 17 mmHg) upon emergence. The bradycardia and hypotension appeared to be vagally mediated, since both these responses were blocked with atropine pre-treatment. These data demonstrate that the mouse exhibits a robust diving response upon voluntary submersion into water.


Heart rate Interbeat interval Blood pressure Dive Reflex 



The authors would like to thank Maia Hare and Cordelia Chan for their help in acquiring some of the data in this work. The authors also thank the animal care staff at Williams College. We also thank the divisional funding resource at Williams College for supporting this work.


The work was supported by an internal grant from Williams College.

Supplementary material

Supplementary material 1 (MP4 24884 kb)


  1. Baranova TI, Berlov DN, Glotov OS, Korf EA, Minigalin AD, Mitrofanova AV, Ahmetov II, Glotov AS (2017) Genetic determination of the vascular reactions in humans in response to the diving reflex. Am J Physiol Heart Circ Physiol 312:H622–H631PubMedGoogle Scholar
  2. Blix AS, Folkow B (1983) Cardiovascular adjustments to diving in mammals and birds. In: Handbook of physiology. The cardiovascular system. Peripheral circulation and organ blood flow, vol III, chap 25. American Physiological Society, Bethesda, pp 917–945Google Scholar
  3. Butler PJ, Jones DR (1997) Physiology of diving of birds and mammals. Physiol Rev 77:837–899PubMedGoogle Scholar
  4. Butz Genelle M, Davisson Robin L (2001) Long-term telemetric measurement of cardiovascular parameters in awake mice: a physiological genomics tool. Physiol Genomics 5:89–97PubMedGoogle Scholar
  5. Cerri M (2017) The central control of energy expenditure: exploiting torpor for medical applications. Annu Rev Physiol 79:167–186PubMedGoogle Scholar
  6. Chouker A, Bereiter-Hahn J, Singer D, Heldmaier G (2019) Hibernating astronauts-science or fiction? Pflugers Arch 471:819–828PubMedGoogle Scholar
  7. Cryan JF, Mombereau C (2004) In search of a depressed mouse: utility of models for studying depression-related behavior in genetically modified mice. Mol Psychiatry 9:326–357PubMedGoogle Scholar
  8. Drummond PC, Jones DR (1979) The initiation and maintenance of bradycardia in a diving mammal, the muskrat, Ondatra zibethica. J Physiol 290:253–271PubMedPubMedCentralGoogle Scholar
  9. Foster GE, Sheel AW (2005) The human diving response, its function, and its control. Scand J Med Sci Sports 15:3–12PubMedGoogle Scholar
  10. Furilla RA, Jones David R (1987) The relationship between dive and pre-dive heart rates in restrained and free dives by diving ducks. J Exp Biol 127:333–348Google Scholar
  11. Griko Yuri, Regan Matthew D (2018) Synthetic torpor: a method for safely and practically transporting experimental animals aboard spaceflight missions to deep space. Life Sci Space Res 16:101–107Google Scholar
  12. Harris MB, Milsom WK (1995) Parasympathetic influence on heart rate in euthermic and hibernating ground squirrels. J Exp Biol 198:931–937PubMedGoogle Scholar
  13. Hiebert Sara M, Burch Elliot (2003) Simulated human diving and heart rate: making the most of the diving response as a laboratory exercise. Adv Physiol Educ 27:130–145PubMedGoogle Scholar
  14. Ilardo MA, Moltke I, Korneliussen TS, Cheng J, Stern AJ, Racimo F, de Barros Damgaard P, Sikora M, Seguin-Orlando A, Rasmussen S, van den Munckhof ICL, Ter Horst R, Joosten LAB, Netea MG, Salingkat S, Nielsen R, Willerslev E (2018) Physiological and genetic adaptations to diving in sea nomads. Cell 173:569-80.e15Google Scholar
  15. Irving Laurence, Scholander PF, Grinnell SW (1942) The regulation of arterial blood pressure in the seal during diving. Am J Physiol Leg Content 135:557–566Google Scholar
  16. Jones David R, West Nigel H, Bamford Owen S, Drummond Peter C, Lord Raymond A (1982) The effect of the stress of forcible submergence on the diving response in muskrats (Ondatra zibethica). Can J Zool 60:187–193Google Scholar
  17. Kaczmarek J, Reichmuth C, McDonald BI, Kristensen JH, Larson J, Johansson F, Sullivan JL, Madsen PT (2018) Drivers of the dive response in pinnipeds; apnea, submergence or temperature? J Exp Biol 221:jeb176545. CrossRefPubMedGoogle Scholar
  18. Lin YC (1974) Autonomic nervous control of cardiovascular response during diving in the rat. Am J Physiol 227:601–605PubMedGoogle Scholar
  19. Lyman CP, O’Brien RC (1960) Circulatory changes in the thirteen-lined ground squirrel during the hibernating cycle. Bull Mus Comp Zool Harv 124:353–372Google Scholar
  20. MacArthur Robert A, Karpan Cindy M (1989) Heart rates of muskrats diving under simulated field conditions: persistence of the bradycardia response and factors modifying its expression. Can J Zool 67:1783–1792Google Scholar
  21. Mattson DL (2001) Comparison of arterial blood pressure in different strains of mice. Am J Hypertens 14:405–408PubMedGoogle Scholar
  22. McCulloch PF (2012) Animal models for investigating the central control of the Mammalian diving response. Front Physiol 3:169PubMedPubMedCentralGoogle Scholar
  23. McCulloch PF (2014) Training rats to voluntarily dive underwater: investigations of the mammalian diving response. J Vis Exp 12(93):e52093. CrossRefGoogle Scholar
  24. McCulloch PF, Ollenberger GP, Bekar LK, West NH (1997) Trigeminal and chemoreceptor contributions to bradycardia during voluntary dives in rats. Am J Physiol 273:R814–R822PubMedGoogle Scholar
  25. McCulloch PF, Dinovo KM, Connolly TM (2010) The cardiovascular and endocrine responses to voluntary and forced diving in trained and untrained rats. Am J Physiol Regul Integr Comp Physiol 298:R224–R234PubMedGoogle Scholar
  26. McDonald BI, Ponganis PJ (2014) Deep-diving sea lions exhibit extreme bradycardia in long-duration dives. J Exp Biol 217:1525–1534PubMedGoogle Scholar
  27. Meir JU, Stockard TK, Williams CL, Ponganis KV, Ponganis PJ (2008) Heart rate regulation and extreme bradycardia in diving emperor penguins. J Exp Biol 211:1169–1179PubMedGoogle Scholar
  28. Milsom WK, Zimmer MB, Harris MB (2001) Vagal control of cardiorespiratory function in hibernation. Exp Physiol 86:791–796PubMedGoogle Scholar
  29. Morhardt JE (1970) Heart rates, breathing rates and effects of atropine and acetylcholine on white-footed mice (Peromyscus) during daily torpor. Comp Biochem Physiol 33:441–457PubMedGoogle Scholar
  30. Murdaugh HV Jr, Seabury JC, Mitchell WL (1961) Electrocardiogram of the diving seal. Circ Res 9:358–361PubMedGoogle Scholar
  31. Nordeen CA, Martin SL (2019) Engineering human stasis for long-duration spaceflight. Physiology (Bethesda) 34:101–111Google Scholar
  32. Panneton W Michael (2013) The mammalian diving response: an enigmatic reflex to preserve life? Physiology 28:284–297PubMedGoogle Scholar
  33. Panneton WM, Gan Q, Le J, Livergood RS, Clercand P, Juric R (2012) Activation of brainstem neurons by underwater diving in the rat. Front Physiol 3:111PubMedPubMedCentralGoogle Scholar
  34. Paredes SD, Sanchez S, Rial RV, Rodriguez AB, Barriga C (2005) Changes in behaviour and in the circadian rhythms of melatonin and corticosterone in rats subjected to a forced-swimming test. J Appl Biomed 3:47–57Google Scholar
  35. Paton Julian F R, Nalivaiko Eugene, Boscan Pedro, Pickering Anthony E (2006) Reflexly evoked coactivation of cardiac vagal and sympathetic motor outflows: observations and functional implications. Clin Exp Pharmacol Physiol 33:1245–1250PubMedGoogle Scholar
  36. Petit G, Koller D, Summerer L, Heldmaier G, Vyazovskiy VV, Cerri M, Henning RH (2018) Hibernation and Torpor: prospects for human spaceflight. In: Seedhouse Erik, Shayler David J (eds) Handbook of Life support systems for spacecraft and extraterrestrial habitats. Springer International Publishing, ChamGoogle Scholar
  37. Ponganis Paul J (2019) State of the art review: from the seaside to the bedside: insights from comparative diving physiology into respiratory, sleep and critical care. Thorax 74:512–518PubMedGoogle Scholar
  38. Ponganis PJ, McDonald BI, Tift MS, Williams CL (2017) Heart rate regulation in diving sea lions: the vagus nerve rules. J Exp Biol 220:1372–1381PubMedGoogle Scholar
  39. Scholander PF (1940) Experimental investigations on the respiratory function in diving mammals and birds. Hvalrådets Skrifter 22:1–131Google Scholar
  40. Signore PE, Jones DR (1995) Effect of pharmacological blockade on cardiovascular responses to voluntary and forced diving in muskrats. J Exp Biol 198:2307–2315PubMedGoogle Scholar
  41. Smith G, Morgans A, Taylor DM, Cameron P (2012) Use of the human dive reflex for the management of supraventricular tachycardia: a review of the literature. Emerg Med J 29:611–616PubMedGoogle Scholar
  42. Swoap Steven J, Gutilla Margaret J (2009) Cardiovascular changes during daily torpor in the laboratory mouse. Am J Physiol Regul Integr Comp Physiol 297:R769–R774PubMedPubMedCentralGoogle Scholar
  43. Swoap Steven J, Michael Overton J, Garber Graham (2004) Effect of ambient temperature on cardiovascular parameters in rats and mice: a comparative approach. Am J Physiol Regul Integr Comp Physiol 287:R391–R396PubMedGoogle Scholar
  44. Yavari P, McCulloch PF, Panneton WM (1996) Trigeminally-mediated alteration of cardiorespiratory rhythms during nasal application of carbon dioxide in the rat. J Auton Nerv Syst 61:195–200PubMedGoogle Scholar
  45. Zosky GR (2002) The parasympathetic nervous system: its role during torpor in the fat-tailed dunnart (Sminthopsis crassicaudata). J Comp Physiol [B] 172:677–684Google Scholar
  46. Zosky Graeme R, Larcombe Alexander N (2003) The parasympathetic nervous system and its influence on heart rate in torpid western pygmy possums, Cercatetus concinnus (Marsupialia: Burramyidae). Zoology 106:143–150PubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of BiologyWilliams CollegeWilliamstownUSA
  2. 2.Molecular and Integrative Physiology Graduate ProgramUniversity of MichiganAnn ArborUSA

Personalised recommendations