Journal of Comparative Physiology A

, Volume 199, Issue 3, pp 183–189 | Cite as

Evaluation of two minimally invasive techniques for electroencephalogram recording in wild or freely behaving animals

  • M. F. Scriba
  • W. M. Harmening
  • C. Mettke-Hofmann
  • A. L. Vyssotski
  • A. Roulin
  • H. Wagner
  • N. C. Rattenborg
Original Paper

Abstract

Insight into the function of sleep may be gained by studying animals in the ecological context in which sleep evolved. Until recently, technological constraints prevented electroencephalogram (EEG) studies of animals sleeping in the wild. However, the recent development of a small recorder (Neurologger 2) that animals can carry on their head permitted the first recordings of sleep in nature. To facilitate sleep studies in the field and to improve the welfare of experimental animals, herein, we test the feasibility of using minimally invasive surface and subcutaneous electrodes to record the EEG in barn owls. The EEG and behaviour of four adult owls in captivity and of four chicks in a nest box in the field were recorded. We scored a 24-h period for each adult bird for wakefulness, slow-wave sleep (SWS), and rapid-eye movement (REM) sleep using 4 s epochs. Although the quality and stability of the EEG signals recorded via subcutaneous electrodes were higher when compared to surface electrodes, the owls’ state was readily identifiable using either electrode type. On average, the four adult owls spent 13.28 h awake, 9.64 h in SWS, and 1.05 h in REM sleep. We demonstrate that minimally invasive methods can be used to measure EEG-defined wakefulness, SWS, and REM sleep in owls and probably other animals.

Keywords

EEG recording method Barn owl Surface electrodes Subcutaneous electrodes Sleep 

Abbreviations

EEG

Electroencephalogram

SWS

Slow-wave sleep

TST

Total sleep time

REM

Rapid-eye movement

Supplementary material

359_2012_779_MOESM1_ESM.mpg (906 kb)
Video 1 Adult barn owl in captivity during slow-wave sleep and rapid-eye movement (REM) sleep. At the beginning of the REM episode one can see the typical reduction in muscle tone when the barn owl drops its head (MPG 906 kb)

References

  1. Allison T (1972) Comparative and evolutionary aspects of sleep. In: Chase MH (ed) Perspectives in the brain sciences: the sleeping brain. Brain Information Service, Los Angeles, pp 1–57Google Scholar
  2. Bell FR, Itabisashi T (1973) The electroencephalogram of sheep and goats with special reference to rumination. Physiol Behav 11:503–514PubMedCrossRefGoogle Scholar
  3. Berger RJ, Walker JM (1972) Sleep in the burrowing owl (Speotyto cunicularia hypugaea). Behav Biol 7:183–194PubMedCrossRefGoogle Scholar
  4. Campbell IG, Feinberg I (2009) Longitudinal trajectories of non-rapid eye movement delta and theta EEG as indicators of adolescent brain maturation. Proc Natl Acad Sci 106:5177–5180PubMedCrossRefGoogle Scholar
  5. Cooper RG, Horbańczuk JO, Villegas-Vizcaíno R, Kennou Sebei S, Faki Mohammed AE, Mahrose KMA (2010) Wild ostrich (Struthio camelus) ecology and physiology. Trop Anim Health Prod 42:363–373Google Scholar
  6. Erkert HG (1969) Die Bedeutung des Lichtsinnes für Aktivität und Raumorientierung der Schleiereule (Tyto alba guttata Brehm). Z Vergl Physiol 64:37–70Google Scholar
  7. Galvão de Moura Filho AG, Huggins SE, Lines SG (1983) Sleep and waking in the three-toed sloth, Bradypus tridactylus. Comp Biochem Physiol A 76:345–355CrossRefGoogle Scholar
  8. Ives JR (2005) New chronic EEG electrode for critical/intensive care unit monitoring. J Clin Neurophysiol 22:119–123PubMedCrossRefGoogle Scholar
  9. Karmanova IG, Churnosov EV (1974) Electrophysiological studies on the diurnal rhythm of sleep and wakefulness in owls. J Evol Biochem Physiol 10:48–57Google Scholar
  10. Kurth S, Ringli M, Geiger A, LeBourgeois M, Jenni OG, Huber R (2010) Mapping of cortical activity in the first two decades of life: a high-density sleep electroencephalogram study. J Neurosci 30:13211–13219PubMedCrossRefGoogle Scholar
  11. Lesku JA, Bark RJ, Martinez-Gonzalez D, Rattenborg NC, Amlaner CJ, Lima SL (2008) Predator-induced plasticity in sleep architecture in wild-caught Norway rats (Rattus norvegicus). Behav Brain Res 189:298–305PubMedCrossRefGoogle Scholar
  12. Lesku JA, Roth TC, Rattenborg NC, Amlaner CJ, Lima SL (2009) History and future of comparative analyses in sleep research. Neurosci Biobehav Rev 33:1024–1036PubMedCrossRefGoogle Scholar
  13. Lesku JA, Meyer LCR, Fuller A, Maloney SK, Dell’Omo G, Vyssotski AL, Rattenborg NC (2011) Ostriches sleep like platypuses. PLoS One 6:e23203PubMedCrossRefGoogle Scholar
  14. Martinez-Gonzalez D, Lesku JA, Rattenborg NC (2008) Increased EEG spectral power density during sleep following short-term sleep deprivation in pigeons (Columba livia): evidence for avian sleep homeostasis. J Sleep Res 17:140–153PubMedCrossRefGoogle Scholar
  15. Paulson G (1964) The avian EEG: an artifact associated with ocular movement. Electroencephalogr Clin Neurophysiol 16:611–613PubMedCrossRefGoogle Scholar
  16. Rattenborg NC, Amlaner CJ, Lima SL (2000) Behavioral, neurophysiological and evolutionary perspectives on unihemispheric sleep. Neurosci Biobehav Rev 24:817–842PubMedCrossRefGoogle Scholar
  17. Rattenborg NC, Voirin B, Vyssotski AL, Kays RW, Spoelstra K, Kuemmeth F, Heidrich W, Wikelski M (2008) Sleeping outside the box: electroencephalographic measures of sleep in sloths inhabiting a rainforest. Biol Lett 4:402–405PubMedCrossRefGoogle Scholar
  18. Ruckebusch Y (1972) The relevance of drowsiness in the circadian cycle of farm animals. Anim Behav 20:637–643PubMedCrossRefGoogle Scholar
  19. Steinbach MJ, Money KE (1973) Eye movements of the owl. Vis Res 13:889–891PubMedCrossRefGoogle Scholar
  20. Šušić VT, Kovačević RM (1973) Sleep patterns in the owl Strix aluco. Physiol Behav 11:313–317PubMedCrossRefGoogle Scholar
  21. Taylor I (2004) Barn owls: predator–prey relationships and conservation. Cambridge University Press, CambridgeGoogle Scholar
  22. Tobler I (2005) Phylogeny of sleep regulation. In: Kryger MH, Roth T, Dement WC (eds) Principles and practice of sleep medicine, 4th edn. Elsevier Saunders, Philadelphia, pp 77–90CrossRefGoogle Scholar
  23. Vyssotski AL, Dell’Omo G, Dell’Ariccia G, Abramchuk AN, Serkov AN, Latanov AV, Loizzo A, Wolfer DP, Lipp H-P (2009) EEG responses to visual landmarks in flying pigeons. Curr Biol 19:1159–1166PubMedCrossRefGoogle Scholar
  24. Wagner H, Frost B (1993) Disparity-sensitive cells in the owl have a characteristic disparity. Nature 364:79–796CrossRefGoogle Scholar
  25. Wagner H, Asadollahi A, Bremen P, Endler F, Vonderschen K, von Campenhausen M (2007) Distribution of interaural time difference in the barn owl’s inferior colliculus in the low- and high-frequency ranges. J Neurosci 27:4191–4200PubMedCrossRefGoogle Scholar
  26. Winkowski DE, Knudsen EI (2007) Top-down control of multimodal sensitivity in the barn owl optic tectum. J Neurosci 27:13279–13291PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • M. F. Scriba
    • 1
    • 2
  • W. M. Harmening
    • 3
    • 4
  • C. Mettke-Hofmann
    • 5
  • A. L. Vyssotski
    • 6
  • A. Roulin
    • 2
  • H. Wagner
    • 3
  • N. C. Rattenborg
    • 1
  1. 1.Avian Sleep GroupMax Planck Institute for OrnithologySeewiesenGermany
  2. 2.Department of Ecology and EvolutionUniversity of LausanneLausanneSwitzerland
  3. 3.Department of Zoology and Animal PhysiologyRWTHAachenGermany
  4. 4.School of OptometryUniversity of CaliforniaBerkeleyUSA
  5. 5.School of Natural Sciences and PsychologyLiverpool John Moores UniversityLiverpoolUK
  6. 6.Institute of NeuroinformaticsUniversity of Zürich/ETHZurichSwitzerland

Personalised recommendations