Hyperthermia-Induced Changes in EEG of Anesthetized Mice Subjected to Passive Heat Exposure
Carmen de Labra, Jose L Pardo-Vazquez, Javier Cudeiro, Casto Rivadulla, Carmen de Labra, Jose L Pardo-Vazquez, Javier Cudeiro, Casto Rivadulla
Abstract
Currently, the role of hypothermia in electroencephalography (EEG) is well-established. However, few studies have investigated the effect of hyperthermia on EEG, an important physiological parameter governing brain function. The aim of this work was to determine how neuronal activity in anesthetized mice is affected when the temperature rises above the physiological threshold mandatory to maintain the normal body functions. In this study, a temperature-elevation protocol, from 37 to 42°C, was applied to four female mice of 2-3 months old while EEG was recorded simultaneously. We found that hyperthermia reduces EEG amplitude by 4.36% when rising from 37 to 38 degrees and by 24.33% when it is increased to 42 degrees. Likewise, increasing the body temperature produces a very large impact on the EEG spectral parameters, reducing the frequency power at the delta, theta, alpha, and beta bands. Our results show that hyperthermia has a global effect on the EEG, being able to change the electrical activity of the brain.
Keywords: anesthetized animal; electroencephalography; hyperthermia; mice; physiology.
Conflict of interest statement
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Copyright © 2021 de Labra, Pardo-Vazquez, Cudeiro and Rivadulla.
Figures
References
- Akeju O., Westover M., Pavone K., Sampson A., Hartnack K. E., Brown E., et al. (2014). Effects of sevoflurane and propofol on frontal electroencephalogram power and coherence. Anesthesiology 121 990–998. 10.1097/aln.0000000000000436
- Barlogie B., Corry P. M., Yip E., Lippman L., Johnston D. A., Khalil K., et al. (1979). Total-body hyperthermia with and without chemotherapy for advanced human neoplasms. Cancer Res. 39 1481–1489.
- Brown E. N., Purdon P. L., Van Dort C. J. (2011). General anesthesia and altered states of arousal: a systems neuroscience analysis. Annu. Rev. Neurosci. 34 601–628. 10.1146/annurev-neuro-060909-153200
- Cabral R., Prior P. F., Scott D. F., Brierley J. B. (1977). Reversible profound depression of cerebral electrical activity in hyperthermia. Electroencephalogr. Clin. Neurophysiol. 42 697–701. 10.1016/0013-4694(77)90286-3
- Cambiaghi M., Grosso A., Likhtik E., Mazziotti R., Concina G., Renna A., et al. (2016). Higher-Order sensory cortex drives Basolateral amygdala activity during the recall of remote, but not recently learned fearful memories. J. Neurosci. 36 1647–1659. 10.1523/jneurosci.2351-15.2016
- Cannon J., McCarthy M., Lee S., Lee J. H., Börgers C., Whittington M., et al. (2014). Neurosystems: brain rhythms and cognitive processing. Eur. J. Neurosci. 39 705–719. 10.1111/ejn.12453
- Crepeau A. M., Britton J., Fugate J., Rabinstein A., Wijdicks E. (2015). Electroencephalography in survivors of cardiac arrest: comparing pre- and post-therapeutic hypothermia eras. Neurocrit. Care 22 165–172. 10.1007/s12028-014-0018-4
- Dubois M., Coppola R., Buchsbaum M. S., Lees D. E. (1981). Somatosensory evoked potentials during whole body hyperthermia in humans. Electroencephalogr. Clin. Neurophysiol. 52 157–162. 10.1016/0013-4694(81)90163-2
- Dubois M., Sato S., Lees D., Bull J., Smith R., White B. G., et al. (1980). Electroencephalographic changes during whole body hyperthermia in humans. Electroencephalogr. Clin. Neurophysiol. 50 486–495. 10.1016/0013-4694(80)90015-2
- Faust O., Acharya U. R., Adeli H., Adeli A. (2015). Wavelet-based EEG processing for computer-aided seizure detection and epilepsy diagnosis. Seizure 26 56–64. 10.1016/j.seizure.2015.01.012
- Fingelkurts A. A., Bagnato S., Boccagni C., Galardi G. (2013). The value of spontaneous EEG oscillations in distinguishing patients in vegetative and minimally conscious states. Suppl. Clin. Neurophysiol. 62 81–99. 10.1016/b978-0-7020-5307-8.00005-3
- Fransen A. M. M., Dimitriadis G., van Ede F., Maris E. (2016). Distinct alpha and beta band rhythms over rat somatosensory cortex with similar properties as in humans. J. Neurophysiol. 115 3030–3044. 10.1152/jn.00507.2015
- Freye E. (1990). “Anesthesia and the EEG,” in Cerebral Monitoring in the Operating Room and the Intensive Care Unit. Developments in Critical Care Medicine and Anesthesiology, Vol. 22 ed. Freye E. (Dordrecht: Springer; ). 10.1007/978-94-009-1886-3_4
- Fries P. (2009). Neuronal gamma-band synchronization as a fundamental process in cortical computation. Annu. Rev. Neurosci. 32 209–224. 10.1146/annurev.neuro.051508.135603
- Gaenshirt H., Krenkel W., Zylka W. (1954). The electrocorticogram of the cat’s brain at temperatures between 40 degrees C. and 20 degrees C. Electroencephalogr. Clin. Neurophysiol. 6 409–413.
- Gaoua N., Racinais S., Grantham J., El Massioui F. (2011). Alterations in cognitive performance during passive hyperthermia are task dependent. Int. J. Hyperthermia 27 1–9. 10.3109/02656736.2010.516305
- Gold S., Cahani M., Sohmer H., Horowitz M., Shahar A. (1985). Effects of body temperature elevation on auditory nerve-brain-stem evoked responses and EEGs in rats. Electroencephalogr. Clin. Neurophysiol. 60 146–153. 10.1016/0013-4694(85)90021-5
- Hagihira S. (2015). Changes in the electroencephalogram during anaesthesia and their physiological basis. Br. J. Anaesth. 115 i27–i31.
- Hancock P. A., Vasmatzidis I. (2003). Effects of heat stress on cognitive performance: the current state of knowledge. Int. J. Hyperthermia 19 355–372. 10.1080/0265673021000054630
- Jia X., Kohn A. (2011). Gamma rhythms in the brain. PLoS Biol. 9:e1001045. 10.1371/journal.pbio.1001045
- Kiyatkin E. A. (2007). Physiological and pathological brain hyperthermia. Prog. Brain Res. 162 219–243. 10.1016/s0079-6123(06)62012-8
- Krol L. R. (2021). Permutation Test, GitHub. Available online at: (accessed February 5, 2021).
- Kubota Y., Nakamoto H., Egawa S., Kawamata T. (2018). Continuous EEG monitoring in ICU. J. Intensive Care 6:39. 10.1186/s40560-018-0310-z
- Lifshitz A., López M., Fiorelli S., Medina E., Osuna G., Halabe J. (1987). The electroencephalogram in adult patients with fever. Clin. Electroencephalogr. 18 85–88.
- Lin T. Y., Healey M. M., Finn M. F., Greenblatt M. (1953). EEG changes during fever produced by inductothermy (fever cabinet) in patients with neurosyphilis. Electroencephalogr. Clin. Neurophysiol. 5 217–224. 10.1016/0013-4694(53)90007-8
- Lundqvist M., Rose J., Herman P., Brincat S., Buschman T. J., Miller E. (2016). Gamma and beta bursts underlie working memory. Neuron 90 152–164. 10.1016/j.neuron.2016.02.028
- Maris E., Oostenveld R. (2007). Nonparametric statistical testing of EEG- and MEG-data. J. Neurosci. Methods 164 177–190. 10.1016/j.jneumeth.2007.03.024
- Mrozek S., Vardon F., Geeraerts T. (2012). Brain temperature: physiology and pathophysiology after brain injury. Anesthesiol. Res. Pract. 2012:989487. 10.1155/2012/989487
- Oakley J. C., Kalume F., Yu F., Scheuer T., Catterall W. (2009). Temperature- and age-dependent seizures in a mouse model of severe myoclonic epilepsy in infancy. Proc. Natl. Acad. Sci. U.S.A. 106 3994–3999. 10.1073/pnas.0813330106
- Pearcy W. C., Virtue R. W. (1959). The electroencephalogram in hypothermia with circulatory arrest. Anesthesiology 20 341–347. 10.1097/00000542-195905000-00014
- Purdon P. L., Sampson A., Pavone K. J., Brown E. N. (2015). Clinical electroencephalography for anesthesiologists: Part I: background and basic signatures. Anesthesiology 123 937–960.
- Racinais S., Gaoua N., Grantham J. (2008). Hyperthermia impairs short-term memory and peripheral motor drive transmission. J. Physiol. 586 4751–4762. 10.1113/jphysiol.2008.157420
- Reilly E. L., Barlogie B., Seward M. A., Corry P. M., Rigor B., Yip E. (1980). The persistence of EEG activity with prolonged induced hyperthermic fever. Clin. Electroencephalogr. 11 22–27. 10.1177/155005948001100104
- Ricobaraza A., Mora-Jimenez L., Puerta E., Sanchez-Carpintero R., Mingorance A., Artieda J., et al. (2019). Epilepsy and neuropsychiatric comorbidities in mice carrying a recurrent Dravet syndrome SCN1A missense mutation. Sci. Rep. 9:14172. 10.1038/s41598-019-50627-w
- Sakoh M., Gjedde A. (2003). Neuroprotection in hypothermia linked to redistribution of oxygen in brain. Am. J. Physiol. Heart Circ. Physiol. 285 H17–H25.
- Sanchez-Vives M. V., Mattia M. (2014). Slow wave activity as the default mode of the cerebral cortex. Arch. Ital. Biol. 152 2–3.
- Sanchez-Vives M. V., Massimini M., Mattia M. (2017). Shaping the default activity pattern of the cortical network. Neuron 94 993–1001. 10.1016/j.neuron.2017.05.015
- Sminia P., van der Zee J., Wondergem J., Haveman J. (1994). Effect of hyperthermia on the central nervous system: a review. Int. J. Hyperthermia 10 1–30. 10.3109/02656739409009328
- Sun G., Qian S., Jiang Q., Liu K., Li B., Li M., et al. (2013). Hyperthermia-Induced disruption of functional connectivity in the human brain network. PLoS One 8:e61157. 10.1371/journal.pone.0061157
- Ten Cate J., Horsten G. P. M., Koopman L. J. (1949). The influence of the body temperature on the EEG of the rat. Electroencephalogr. Clin. Neurophysiol. 1 231–235. 10.1016/0013-4694(49)90181-9
- van Gassen K. L., Hessel E. V., Ramakers G. M., Notenboom R. G., Wolterink-Donselaar I. G., Brakkee J. H., et al. (2008). Characterization of febrile seizures and febrile seizure susceptibility in mouse inbred strains. Genes Brain Behav. 7 578–586. 10.1111/j.1601-183x.2008.00393.x
- Wang X. J. (2010). Neurophysiological and computational principles of cortical rhythms in cognition. Physiol. Rev. 90 1195–1268. 10.1152/physrev.00035.2008
Source: PubMed