Experimental Brain Research

, Volume 232, Issue 8, pp 2591–2599 | Cite as

Provocative motion causes fall in brain temperature and affects sleep in rats

  • Flavia Del Vecchio
  • Eugene Nalivaiko
  • Matteo Cerri
  • Marco Luppi
  • Roberto Amici
Research Article
First Online:
Received:
Accepted:

Abstract

Neural substrate of nausea is poorly understood, contrasting the wealth of knowledge about the emetic reflex. One of the reasons for this knowledge deficit is limited number and face validity of animal models of nausea. Our aim was to search for new physiological correlates of nausea in rats. Specifically, we addressed the question whether provocative motion (40-min rotation at 0.5 Hz) affects sleep architecture, brain temperature, heart rate (HR) and arterial pressure. Six adult male Sprague–Dawley rats were instrumented for recordings of EEG, nuchal electromyographic, hypothalamic temperature and arterial pressure. Provocative motion had the following effects: (1) total abolition of REM sleep during rotation and its substantial reduction during the first hour post-rotation (from 20 ± 3 to 5 ± 1.5 %); (2) reduction in NREM sleep, both during rotation (from 57 ± 6 to 19 ± 5 %) and during the first hour post-rotation (from 56 ± 3 to 41 ± 9 %); (3) fall in the brain temperature (from 37.1 ± 0.1 to 36.0 ± 0.1 °C); and (4) reduction in HR (from 375 ± 6 to 327 ± 7 bpm); arterial pressure was not affected. Ondansetron, a 5-HT3 antagonist, had no major effect on all observed parameters during both baseline and provocative motion. We conclude that in rats, provocative motion causes prolonged arousing effects, however without evidence of sympathetic activation that usually accompanies heightened arousal. Motion-induced fall in the brain temperature complements and extends our previous observations in rats and suggests that similar to humans, provocative motion triggers coordinated thermoregulatory response, leading to hypothermia in this species.

Keywords

Provocative motion Motion sickness Sleep Brain temperature Cardiovascular 
This is a preview of subscription content, log in to check access.

References

  1. Bayer L, Constantinescu I, Perrig S, Vienne J, Vidal PP, Muhlethaler M, Schwartz S (2011) Rocking synchronizes brain waves during a short nap. Curr Biol 21:R461–R462. doi: 10.1016/j.cub.2011.05.012 PubMedCrossRefGoogle Scholar
  2. Cerri M, Ocampo-Garces A, Amici R et al (2005) Cold exposure and sleep in the rat: effects on sleep architecture and the electroencephalogram. Sleep 28:694–705PubMedGoogle Scholar
  3. Cheung B, Hofer K (2001) Coriolis-induced cutaneous blood flow increase in the forearm and calf. Brain Res Bull 54:609–618PubMedCrossRefGoogle Scholar
  4. Cheung B, Nakashima AM, Hofer KD (2011) Various anti-motion sickness drugs and core body temperature changes. Aviat Space Environ Med 82:409–415PubMedCrossRefGoogle Scholar
  5. Di Maio M, Bria E, Banna GL, Puglisi F, Garassino MC, Lorusso D, Perrone F (2013) Prevention of chemotherapy-induced nausea and vomiting and the role of neurokinin 1 inhibitors: from guidelines to clinical practice in solid tumors. Anticancer Drugs 24:99–111. doi: 10.1097/CAD.0b013e328359d7ba PubMedCrossRefGoogle Scholar
  6. Fisher RD, Rentschler RE, Nelson JC, Godfrey TE, Wilbur DW (1982) Elevation of plasma antidiuretic hormones (ADH) associated with chemotherapy-induced emesis in man. Cancer Treat Rep 66:25–29PubMedGoogle Scholar
  7. Fox RA, Keil LC, Daunton NG, Crampton GH, Lucot J (1987) Vasopressin and motion sickness in cats. Aviat Space Environ Med 58:A143–A147PubMedGoogle Scholar
  8. Franken P, Dijk DJ, Tobler I, Borbely AA (1991) Sleep deprivation in rats: effects on EEG power spectra, vigilance states, and cortical temperature. Am J Physiol 261:R198–R208PubMedGoogle Scholar
  9. Gao BO, Franken P, Tobler I, Borbely AA (1995) Effect of elevated ambient temperature on sleep, EEG spectra, and brain temperature in the rat. Am J Physiol 268:R1365–R1373PubMedGoogle Scholar
  10. Graybiel A, Knepton J (1976) Sopite syndrome: a sometimes sole manifestation of motion sickness. Aviat Space Environ Med 47:873–882PubMedGoogle Scholar
  11. Graybiel A, Lackner JR (1980) Evaluation of the relationship between motion sickness symptomatology and blood pressure, heart rate, and body temperature. Aviat Space Environ Med 51:211–214PubMedGoogle Scholar
  12. Haward BM, Lewis CH, Griffin MJ (2009) Motions and crew responses on an offshore oil production and storage vessel. Appl Ergon 40:904–914. doi: 10.1016/j.apergo.2009.01.001 PubMedCrossRefGoogle Scholar
  13. Hawthorn J, Andrews PL, Ang VT, Jenkins JS (1988) Differential release of vasopressin and oxytocin in response to abdominal vagal afferent stimulation or apomorphine in the ferret. Brain Res 438:193–198PubMedCrossRefGoogle Scholar
  14. Hershkovitz D, Asna N, Shupak A, Kaminski G, Bar R, Tal D (2009) Ondansetron for the prevention of seasickness in susceptible sailors: an evaluation at sea. Aviat Space Environ Med 80:643–646PubMedCrossRefGoogle Scholar
  15. Hornby PJ (2001) Central neurocircuitry associated with emesis. Am J Med 111(Suppl 8A):106S–112SPubMedCrossRefGoogle Scholar
  16. Hu S, Grant WF, Stern RM, Koch KL (1991) Motion sickness severity and physiological correlates during repeated exposures to a rotating optokinetic drum. Aviat Space Environ Med 62:308–314PubMedGoogle Scholar
  17. Ishikawa T, Miyazawa T (1980) Sympathetic responses evoked by vestibular stimulation and their interactions with somato-sympathetic reflexes. J Auton Nerv Syst 1:243–254PubMedCrossRefGoogle Scholar
  18. Kerman IA, Emanuel BA, Yates BJ (2000) Vestibular stimulation leads to distinct hemodynamic patterning. Am J Physiol Regul Integr Comp Physiol 279:R118–R125PubMedGoogle Scholar
  19. Kim YY, Kim HJ, Kim EN, Ko HD, Kim HT (2005) Characteristic changes in the physiological components of cybersickness. Psychophysiology 42:616–625. doi: 10.1111/j.1469-8986.2005.00349.x PubMedGoogle Scholar
  20. Kim J, Napadow V, Kuo B, Barbieri R (2011) A combined HRV-fMRI approach to assess cortical control of cardiovagal modulation by motion sickness. Conf Proc IEEE Eng Med Biol Soc :2825–2828 doi: 10.1109/IEMBS.2011.6090781
  21. Krystal AD, Zammit GK, Wyatt JK et al (2010) The effect of vestibular stimulation in a four-hour sleep phase advance model of transient insomnia. J Clin Sleep Med 6:315–321PubMedCentralPubMedGoogle Scholar
  22. Lacount L, Napadow V, Kuo B, Park K, Kim J, Brown E, Barbieri R (2009) Dynamic cardiovagal response to motion sickness: a point-process heart rate variability study. Comput Cardiol 36:49–52PubMedCentralPubMedGoogle Scholar
  23. Liu YL, Malik N, Sanger GJ, Friedman MI, Andrews PL (2005) Pica—a model of nausea? Species differences in response to cisplatin. Physiol Behav 85:271–277. doi: 10.1016/j.physbeh.2005.04.009 PubMedCrossRefGoogle Scholar
  24. McCaffrey RJ (1985) Appropriateness of kaolin consumption as an index of motion sickness in the rat. Physiol Behav 35:151–156PubMedCrossRefGoogle Scholar
  25. Mitchell D, Laycock JD, Stephens WF (1977) Motion sickness-induced pica in the rat. Am J Clin Nutr 30:147–150PubMedGoogle Scholar
  26. Morrison SF, Nakamura K (2011) Central neural pathways for thermoregulation. Front Biosci (Landmark Ed) 16:74–104CrossRefGoogle Scholar
  27. Navari RM (2013) Management of chemotherapy-induced nausea and vomiting: focus on newer agents and new uses for older agents. Drugs 73:249–262. doi: 10.1007/s40265-013-0019-1 PubMedCrossRefGoogle Scholar
  28. Ngampramuan S, Baumert M, Czippelova B, Nalivaiko E (2013a) Ondansetron prevents changes in respiratory pattern provoked by LiCl: a new approach for studying pro-emetic states in rodents? Neuroscience 246:342–350. doi: 10.1016/j.neuroscience.2013.05.012 PubMedCrossRefGoogle Scholar
  29. Ngampramuan S, Cerri M, Del Veccio F, et al (2013b) Thermoregulatory correlates of nausea in rats and musk shrews. Oncotarget 5. http://www.impactjournals.com/oncotarget/index.php?journal=oncotarget&page=article&op=view&path%5B%5D=1732
  30. Nobel G, Eiken O, Tribukait A, Kolegard R, Mekjavic IB (2006) Motion sickness increases the risk of accidental hypothermia. Eur J Appl Physiol 98:48–55. doi: 10.1007/s00421-006-0217-6 PubMedCrossRefGoogle Scholar
  31. Nobel G, Tribukait A, Mekjavic IB, Eiken O (2012) Effects of motion sickness on thermoregulatory responses in a thermoneutral air environment. Eur J Appl Physiol 112:1717–1723. doi: 10.1007/s00421-011-2142-6 PubMedCrossRefGoogle Scholar
  32. Noble RL (1948) Adaptation to experimental motion sickness in dogs. Am J Physiol 154:443–450PubMedGoogle Scholar
  33. Ootsuka Y, de Menezes RC, Zaretsky DV et al (2009) Brown adipose tissue thermogenesis heats brain and body as part of the brain-coordinated ultradian basic rest-activity cycle. Neuroscience 164:849–861. doi: 10.1016/j.neuroscience.2009.08.013 PubMedCentralPubMedCrossRefGoogle Scholar
  34. Ossenkopp KP (1983) Area postrema lesions in rats enhance the magnitude of body rotation-induced conditioned taste aversions. Behav Neural Biol 38:82–96PubMedCrossRefGoogle Scholar
  35. Ossenkopp KP, Rabi YJ, Eckel LA, Hargreaves EL (1994) Reductions in body temperature and spontaneous activity in rats exposed to horizontal rotation: abolition following chemical labyrinthectomy. Physiol Behav 56:319–324PubMedCrossRefGoogle Scholar
  36. Paxinos G, Watson C (2007) The rat brain in stereotaxic coordinates, rth edition. Elsevier, AmsterdamGoogle Scholar
  37. Perenin MT, Maeda T, Jeannerod M (1972) Are vestibular nuclei responsible for rapid eye movements of paradoxical sleep? Brain Res 43:617–621PubMedCrossRefGoogle Scholar
  38. Pompeiano O, Morrison AR (1965) Vestibular influences during sleep. I. Abolition of the rapid eye movements of desynchronized sleep following vestibular lesions. Arch Ital Biol 103:569–595PubMedGoogle Scholar
  39. Riccio DC, Thach JS Jr (1968) Response suppression produced by vestibular stimulation in the rat. J Exp Anal Behav 11:479–488. doi: 10.1901/jeab.1968.11-479 PubMedCentralPubMedCrossRefGoogle Scholar
  40. Rockstroh B, Johnen M, Elbert T et al (1987) The pattern and habituation of the orienting response in man and rats. Int J Neurosci 37:169–182PubMedCrossRefGoogle Scholar
  41. Romanovsky AA (2007) Thermoregulation: some concepts have changed. Functional architecture of the thermoregulatory system. Am J Physiol Regul Integr Comp Physiol 292:R37–R46. doi: 10.1152/ajpregu.00668.2006 PubMedCrossRefGoogle Scholar
  42. Rowe JW, Shelton RL, Helderman JH, Vestal RE, Robertson GL (1979) Influence of the emetic reflex on vasopressin release in man. Kidney Int 16:729–735PubMedCrossRefGoogle Scholar
  43. Sanger GJ, Andrews PL (2006) Treatment of nausea and vomiting: gaps in our knowledge. Auton Neurosci 129:3–16. doi: 10.1016/j.autneu.2006.07.009 PubMedCrossRefGoogle Scholar
  44. Sanwald JC, Porzio NR, Deane GE, Donovick PJ (1970) The effects of septal and dorsal hippocampal lesions on the cardiac component of the orienting response. Physiol Behav 5:883–888PubMedCrossRefGoogle Scholar
  45. Shido O, Sakurada S, Kohda W, Nagasaka T (1994) Day-night changes of body temperature and feeding activity in heat-acclimated rats. Physiol Behav 55:935–939PubMedCrossRefGoogle Scholar
  46. Stern R, Koch K, Andrews P (2011) Nausea. Oxford University Press, New YorkGoogle Scholar
  47. Sunahara FA, Farewell J, Mintz L, Johnson WH (1987) Pharmacological interventions for motion sickness: cardiovascular effects. Aviat Space Environ Med 58:A270–A276PubMedGoogle Scholar
  48. Suri KB, Crampton GH, Daunton NG (1979) Motion sickness in cats: a symptom rating scale used in laboratory and flight tests. Aviat Space Environ Med 50:614–618PubMedGoogle Scholar
  49. Treisman M (1977) Motion sickness: an evolutionary hypothesis. Science 197:493–495PubMedCrossRefGoogle Scholar
  50. Tuerke KJ, Winters BD, Parker LA (2012) Ondansetron interferes with unconditioned lying-on belly and acquisition of conditioned gaping induced by LiCl as models of nausea-induced behaviors in rats. Physiol Behav 105:856–860. doi: 10.1016/j.physbeh.2011.10.017 PubMedCrossRefGoogle Scholar
  51. Ueno S, Matsuki N, Saito H (1988) Suncus murinus as a new experimental model for motion sickness. Life Sci 43:413–420PubMedCrossRefGoogle Scholar
  52. Verbalis JG, McHale CM, Gardiner TW, Stricker EM (1986) Oxytocin and vasopressin secretion in response to stimuli producing learned taste aversions in rats. Behav Neurosci 100:466–475PubMedCrossRefGoogle Scholar
  53. Wallenstein S, Zucker CL, Fleiss JL (1980) Some statistical methods useful in circulation research. Circ Res 47:1–9PubMedCrossRefGoogle Scholar
  54. Winer BJ, Brown DR, Michels KM (1991) Statistical principles in experimental design. McGraw-Hill, New YorkGoogle Scholar
  55. Woodward S, Tauber ES, Spielmann AJ, Thorpy MJ (1990) Effects of otolithic vestibular stimulation on sleep. Sleep 13:533–537PubMedGoogle Scholar
  56. Yamamoto K, Ngan MP, Takeda N, Yamatodani A, Rudd JA (2004) Differential activity of drugs to induce emesis and pica behavior in Suncus murinus (house musk shrew) and rats. Physiol Behav 83:151–156. doi: 10.1016/j.physbeh.2004.08.006 PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Flavia Del Vecchio
    • 1
  • Eugene Nalivaiko
    • 2
  • Matteo Cerri
    • 1
  • Marco Luppi
    • 1
  • Roberto Amici
    • 1
  1. 1.Department of Biomedical and NeuroMotor SciencesAlma Mater Studiorum University of BolognaBolognaItaly
  2. 2.School of Biomedical Sciences and PharmacyUniversity of NewcastleCallaghanAustralia

Personalised recommendations