Journal of Comparative Physiology A

, Volume 198, Issue 2, pp 119–127 | Cite as

Electroencephalogram bands modulated by vigilance states in an anuran species: a factor analytic approach

  • Guangzhan Fang
  • Qin Chen
  • Jianguo Cui
  • Yezhong Tang
Original Paper


Dramatic changes in neocortical electroencephalogram (EEG) rhythms are associated with the sleep–waking cycle in mammals. Although amphibians are thought to lack a neocortical homologue, changes in rest–activity states occur in these species. In the present study, EEG signals were recorded from the surface of the cerebral hemispheres and midbrain on both sides of the brain in an anuran species, Babina daunchina, using electrodes contacting the meninges in order to measure changes in mean EEG power across behavioral states. Functionally relevant frequency bands were identified using factor analysis. The results indicate that: (1) EEG power was concentrated in four frequency bands during the awake or active state and in three frequency bands during rest; (2) EEG bands in frogs differed substantially from humans, especially in the fast frequency band; (3) bursts similar to mammalian sleep spindles, which occur in non-rapid eye movement mammalian sleep, were observed when frogs were at rest suggesting sleep spindle-like EEG activity appeared prior to the evolution of mammals.


Electroencephalogram (EEG) bands Factor analysis Power spectra Sleep spindle Frog 


  1. Aristakesyan E, Karmanova I (2007) Effect of photostimulation on the wakefulness–sleep cycle in the common frog Rana temporaria. J Evol Biochem Physl Engl Transl 43(2):208–214CrossRefGoogle Scholar
  2. Bakalian MJ, Fernstrom JD (1990) Effects of l-tryptophan and other amino acids on electroencephalographic sleep in the rat. Brain Res 528(2):300–307PubMedCrossRefGoogle Scholar
  3. Balasandaram K, Ramalingam K, Selvarajan V (1997) Bioelectrical activity of brain in Rana tigrina (Daudin) in response to phosalone poisoning. Comp Biochem Physiol C: Pharmacol Toxicol Endocrinol 118(2):229–231CrossRefGoogle Scholar
  4. Basar E, Basar-Eroglu C, Karakas S, Schurmann M (2000) Brain oscillations in perception and memory. Int J Psychophysiol 35(2–3):95–124PubMedCrossRefGoogle Scholar
  5. Basar E, Basar-Eroglu C, Karakas S, Schurmann M (2001) Gamma, alpha, delta, and theta oscillations govern cognitive processes. Int J Psychophysiol 39(2–3):241–248PubMedCrossRefGoogle Scholar
  6. Bjorvatn B, Fagerland S, Ursin R (1998) EEG power densities (0.5–20 Hz) in different sleep–wake stages in rats. Physiol Behav 63(3):413–417PubMedCrossRefGoogle Scholar
  7. Blisard K, Fagin K, Falivena P, Privitera M, Olejniczak P, Harrington D, Taylor K, Scremin O (1994) Experimental seizures in the frog (Rana pipiens). Epilepsy Res 17(1):13–22PubMedCrossRefGoogle Scholar
  8. Buzsaki G, Draguhn A (2004) Neuronal oscillations in cortical networks. Science 304(5679):1926–1929PubMedCrossRefGoogle Scholar
  9. Cohen J (1992) A power primer. Psychol Bull 112(1):155–159PubMedCrossRefGoogle Scholar
  10. Corsi-Cabrera M, Guevara M, Del-Río-Portilla Y, Arce C, Villanueva-Hernández Y (2000) EEG bands during wakefulness, slow-wave and paradoxical sleep as a result of principal component analysis in man. Sleep 23(6):1–7Google Scholar
  11. Corsi-Cabrera M, Pérez-Garci E, Del-Río-Portilla Y, Ugalde E, Guevara M (2001) EEG bands during wakefulness, slow-wave, and paradoxical sleep as a result of principal component analysis in the rat. Sleep 24(4):374–380PubMedGoogle Scholar
  12. Csicsvari J, Jamieson B, Wise KD, Buzsaki G (2003) Mechanisms of gamma oscillations in the hippocampus of the behaving rat. Neuron 37(2):311–322PubMedCrossRefGoogle Scholar
  13. Cui J, Wang Y, Brauth S, Tang Y (2010) A novel female call incites male-female interaction and male–male competition in the Emei music frog, Babina daunchina. Anim Behav 80:181–187CrossRefGoogle Scholar
  14. Engel AK, Fries P, Singer W (2001) Dynamic predictions: oscillations and synchrony in top-down processing. Nat Rev Neurosci 2(10):704–716PubMedCrossRefGoogle Scholar
  15. Fang G, Xia Y, Lai Y, You Z, Yao D (2010) Long-range correlations of different EEG derivations in rats: sleep stage-dependent generators may play a key role. Physiol Meas 31:795–808PubMedCrossRefGoogle Scholar
  16. Grasing K, Szeto H (1992) Diurnal variation in continuous measures of the rat EEG power spectra. Physiol Behav 51(2):249–254PubMedCrossRefGoogle Scholar
  17. Hair J, Anderson R, Tatham R, Black W (1998) Multivariate data analysis. Prentice–Hall, EnglewoodGoogle Scholar
  18. Hobson J (1967a) Electrographic correlates of behavior in the frog with special reference to sleep. Electroencephalogr Clin Neurophysiol 22(2):113–121PubMedCrossRefGoogle Scholar
  19. Hobson J (1967b) Respiration and EEG synchronization in the frog. Nature 213:988–989CrossRefGoogle Scholar
  20. Hobson J, Goin O, Goin C (1968) Electrographic correlates of behaviour in tree frogs. Nature 220:386–387PubMedCrossRefGoogle Scholar
  21. Hoffmann A, Menescal De Oliveira L (1990) Changes in electric activity (EEG) of the telencephalon of conscious toads (Bufo paracnemis) caused by cholinergic stimulation of the mesencephalic tegmentum. Physiol Behav 47(5):857–861PubMedCrossRefGoogle Scholar
  22. Hoffmann A, Romero S, Menescal-de-Oliveira L (1994) The basal midbrain as a region modulating the level of alerting in the toad, Bufo paracnemis. Physiol Behav 55(2):301–306PubMedCrossRefGoogle Scholar
  23. Ismail K (2008) Unravelling factor analysis. Br Med J 11(4):99–102Google Scholar
  24. Karmanova I (1996) Novel about peculiarities of sleep and organization of the wakefulness–sleep cycle in poikilothermal vertebrates. Zh Evol Biokhim Fiziol 32:511–535PubMedGoogle Scholar
  25. Karmanova I, Aristakesyan E, Shilling N (1987) Neurophysiological analysis of hypothalamic mechanisms for the regulation of primary sleep and hypobiosis. Dokl Akad Nauk SSSR 294:245–248PubMedGoogle Scholar
  26. Klimesch W (1999) EEG alpha and theta oscillations reflect cognitive and memory performance: a review and analysis. Brain Res Rev 29(2–3):169–195PubMedCrossRefGoogle Scholar
  27. Kline P (1994) An easy guide to factor analysis. Routledge, LondonGoogle Scholar
  28. Kopell N, Ermentrout G, Whittington M, Traub R (2000) Gamma rhythms and beta rhythms have different synchronization properties. Proc Natl Acad Sci USA 97(4):1867–1872PubMedCrossRefGoogle Scholar
  29. Kostowski W (1967) Pharmacological analysis of bioelectrical activity of the central nervous system of amphibia. I. The effect of some cholinergic and anticholinergic drugs on the frog’s EEG. Brain Res 6(4):783–785PubMedCrossRefGoogle Scholar
  30. Laming P (1982) Electroencephalographic correlates of behavior in the anurans Bufo regularis and Rana temporaria. Behav Neural Biol 34(3):296–306PubMedCrossRefGoogle Scholar
  31. Lancel M, Kerkhof GA (1989) Effects of repeated sleep deprivation in the dark-or light-period on sleep in rats. Physiol Behav 45(2):289–297PubMedCrossRefGoogle Scholar
  32. Merica H, Fortune R (2004) State transitions between wake and sleep, and within the ultradian cycle, with focus on the link to neuronal activity. Sleep Med Rev 8(6):473–485PubMedCrossRefGoogle Scholar
  33. Nunez PL, Cutillo BA (1995) Neocortical dynamics and human EEG rhythms. Oxford University Press, New YorkGoogle Scholar
  34. Ono K, Baba H, Mori K, Sato K (1980) EEG activities during kindling in frog. Int J Neurosci 11(1):9–15PubMedCrossRefGoogle Scholar
  35. Pan WX, McNaughton N (1997) The medial supramammillary nucleus, spatial learning and the frequency of hippocampal theta activity. Brain Res 764(1–2):101–108PubMedCrossRefGoogle Scholar
  36. Pletzer B, Kerschbaum H, Klimesch W (2010) When frequencies never synchronize: the golden mean and the resting EEG. Brain Res 1335:91–102PubMedCrossRefGoogle Scholar
  37. Rechtschaffen A, Kales A (1968) A manual of standardized terminology, technique and scoring system for sleep stages of human subjects. UCLA Brain Information Service, Los AngelesGoogle Scholar
  38. Saastamoinen A, Huupponen E, Varri A, Hasan J, Himanen S (2007) Systematic performance evaluation of a continuous-scale sleep depth measure. Med Eng Phys 29(10):1119–1131PubMedCrossRefGoogle Scholar
  39. Sato K (1969) On the effects of cutaneous stimulations upon EEG, respiratory and muscular activities of frog. Acta Med Nagasaki 13:14–27Google Scholar
  40. Segura E, De Juan A (1966) Electroencephalographic studies in toads. Electroencephalogr Clin Neurophysiol 21(4):373–380PubMedCrossRefGoogle Scholar
  41. Servít Z, Machek J, Fischer J (1965) Electrical activity of the frog brain during electrically induced seizures. A comparative study of the spike and wave complex. Electroencephalogr Clin Neurophysiol 19(2):162–171PubMedCrossRefGoogle Scholar
  42. Smolin L (1962) The origin of the “spontaneous” electrical activity of the frog brain. Bull Exp Biol Med 52(6):1359–1362CrossRefGoogle Scholar
  43. Tauber E (1974) The phylogeny of sleep. In: Weitzman ED (ed) Advances in sleep research. Wiley, New York, pp 133–172Google Scholar
  44. Thut G, Miniussi C (2009) New insights into rhythmic brain activity from TMS–EEG studies. Trends Cogn Sci 13(4):182–189PubMedCrossRefGoogle Scholar
  45. Whishaw I, Vanderwolf C (1971) Hippocampal EEG and behavior: effects of variation in body temperature and relation of EEG to vibrissae movement, swimming and shivering. Physiol Behav 6(4):391–397Google Scholar
  46. Young C, McNaughton N (2009) Coupling of theta oscillations between anterior and posterior midline cortex and with the hippocampus in freely behaving rats. Cereb Cortex 19:24–40PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Guangzhan Fang
    • 1
  • Qin Chen
    • 1
  • Jianguo Cui
    • 1
  • Yezhong Tang
    • 1
  1. 1.Department of Herpetology, Chengdu Institute of BiologyChinese Academy of SciencesChengduPeople’s Republic of China

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