For citation:
Dolinina A. Y., Suleymanova E. M., Kornilov M. V., Sysoeva M. V., Sysoev I. V. Nonlinear properties of the brain theta rhythm. Izvestiya VUZ. Applied Nonlinear Dynamics, 2025, vol. 33, iss. 6, pp. 873-897. DOI: 10.18500/0869-6632-003188, EDN: CNWBIT
Nonlinear properties of the brain theta rhythm
The purpose of this study is to identify nonlinearity of local brain field potential signals during theta rhythm.
Methods. The nonlinearity in the signal is manifested in the synchronous behavior of the fundamental frequency and its higher harmonics; to detect this, skeletons in different frequency ranges were used, the phase synchronization index was calculated and cross-spectral analysis was performed.
Results. The fundamental frequency and the second harmonic in the spectrum during the theta rhythm were identified from multi-hour recordings in 14 animals. Based on the skeletons constructed from these recordings, frequency synchronization between the
fundamental frequency and the second harmonic in the ratio of 2:1 was diagnosed at intervals of up to 10 s in both symmetrical channels. Phase synchronization was also diagnosed in a number of recordings, but at shorter intervals (about 2–4 s).
Conclusion. The study proved that the spectral component observed at the theta-rhythm in healthy laboratory animals in the signals of local brain field potentials at the range containing twice fundamental frequency of the rhythm is indeed the second harmonic of the fundamental frequency. Thus, the theta rhythm is often a significantly nonlinear signal.
- Buzs'aki G. Rhythms of the Brain. Oxford: Oxford University Press; 2006. 464 p DOI: 10.1093/acprof:oso/9780195301069.001.0001.
- Bas ar E, Basar-Eroglu C, Karakas S, Sch"urmann M. Gamma, alpha, delta, and theta oscillations govern cognitive processes. Int. J. Psychophysiol. 2001;39(2-3):241-248 DOI: 10.1016/s0167-8760(00)00145-8.
- Waldhoer M, Bartlett SE, Whistler J L. Opioid receptors. Annu. Rev. Biochem. 2004;73:953-990 DOI: 10.1146/annurev.biochem.73.011303.073940.
- Nozdrachev АD, Barannikova IА, Batuev АS, Kassil VG, Konstantinov АI, Lapitskii VP, Matyushkin DP, Pushkarev Yu P. General Course in Human and Animal Physiology. Book One. Physiology of the Nervous, Muscular, and Sensory Systems. М.: Vysshaya Shkola; 1991. 509 p. (in Russian).
- L'eger D, Debellemaniere E, Rabat A, Bayon V, Benchenane K, Chennaoui M. Slow-Wave Sleep: From the Cell to the Clinic. Sleep Medicine Reviews. 2018;41:113-132 DOI: 10.1016/j.smrv.2018.01.008.
- Vinogradova О S. The Hippocampus and Memory. М.: Nauka; 1975. 332 p.
- Crouzier D, Baubichon D, Bourbon F, Testylier G. Acetylcholine release, EEG spectral analysis, sleep staging and body temperature studies: a multiparametric approach on freely moving rats. J. Neurosci. Methods. 2006;151(2):159-167 DOI: 10.1016/j.jneumeth.2005.07.003.
- Young CK, McNaughton N. Coupling of theta oscillations between anterior and posterior midline cortex and with the hippocampus in freely behaving rats. Cerebral Cortex. 2009;19(1):24-40 DOI: 10.1093/cercor/bhn055.
- Silva AL, Fry WHD, Sweeney C, Trainor B C. Effects of photoperiod and experience on aggressive behavior in female California mice. Behavioural Brain Research. 2010;208(2):528-534 DOI: 10.1016/j.bbr.2009.12.038.
- Green JD, Arduini A A. Hippocampal electrical activity in arousal. Journal of Neurophysiology. 1954;17(6):533-557 DOI: 10.1152/jn.1954.17.6.533.
- Vanderwolf C H. Hippocampal electrical activity and voluntary movement in the rat. Electro-encephalogr. Clin. Neurophysiol. 1969;26(4):407-418 DOI: 10.1016/0013-4694(69)90092-3.
- Buzs'a ki G. Theta rhythm of navigation: link between path integration and landmark navigation, episodic and semantic memory. Hippocampus. 2005;15(7):827-840 DOI: 10.1002/hipo.20113.
- Nunez A, Bu no W.The theta rhythm of the hippocampus: from neuronal and circuit mechanisms to behavior. Front. Cell. Neurosci. 2021;15:649262 DOI: 10.3389/fncel.2021.649262.
- Maurer AP, Vanrhoads SR, Sutherland GR, Lipa P, McNaughton B L. Self-motion and the origin of differential spatial scaling along the septo-temporal axis of the hippocampus. Hippocampus. 2005;15(7):841-852 DOI: 10.1002/hipo.20114.
- Buzs'a ki G, Leung LW, Vanderwolf CH. Cellular bases of hippocampal EEG in the behaving rat. Brain Res. Rev. 1983;6(2):139-171 DOI: 10.1016/0165-0173(83)90037-1.
- Terrazas A, Krause M, Lipa P, Gothard KM, Barnes CA, McNaughton B L. Self-motion and the hippocampal spatial metric. J. Neurosci. 2005;25(35):8085-8096. 10.1523/JNEUROSCI.0693-05.200510.1523/JNEUROSCI.0693-05.2005. 1.
- Czurk'o A, Hirase H, Csicsvari J, Buzs'aki G. Sustained activation of hippocampal pyramidal cells by ‘space clamping’ in a running wheel. Eur. J. Neurosci. 2001;11(1):344-352. 10.1046/j.1460-9568.1999.00446.x10.1046/j.1460-9568.1999.00446.x.
- Sheremet A, Burke SN, Maurer A P. Movement enhances the nonlinearity of hippocampal theta. J. Neurosci. 2016;36(15):4218-4230 DOI: 10.1523/JNEUROSCI.3564-15.2016.
- Harper R M. Frequency changes in hippocampal electrical activity during movement and tonic immobility. Physiol. Behav. 1971;7(1):55-58 DOI: 10.1016/0031-9384(71)90235-6.
- Coenen A M. Frequency analysis of rat hippocampal electrical activity. Physiol. Behav. 1975;14(3):391-394 DOI: 10.1016/0031-9384(75)90053-0.
- Leung LW, Lopes da Silva FH, Wadman W J. Spectral characteristics of the hippocampal EEG in the freely moving rat. Electroencephalogr. Clin. Neurophysiol. 1982;54(2):203-219. . - 22 DOI: 10.1016/0013-4694(82)90162-6.
- Blekhman II, Fradkov AL, Nijmeijer H, Pogromsky AY u. On self-synchronization and controlled synchronization. Systems and Control Letters. 1997;31(5):299-305. DOI: 10.1016/S0167-6911(97)00047-9.
- Blekhman I I. Frequency synchronization and its possible role in microworld phenomena. Autom. Remote Control. 2020;81:1405-1412. DOI: 10.1134/S0005117920080044.
- Tang DY, Dykstra R, Hamilton MW, Heckenberg N R. Stages of chaotic synchronization. Chaos. 1998;8(3):697-701. DOI: 10.1063/1.166352.
- Suleymanova EM, Shangaraeva VA, van Rijn CM, Vinogradova L V. The cannabinoid receptor agonist WIN55.212 reduces consequences of status epilepticus in rats. Neuroscience. 2016;334:191-200. DOI: 10.1016/j.neuroscience.2016.08.004.
- Dolinina AYu, van Rijn CM, Sysoeva MV, Sysoev I V. Detection of spike-wave discharge restarts in genetic rat model based on frequency dynamics. Cybernetics and Physics. 2022;11(3):121-130. DOI: 10.35470/2226-4116-2022-11-3-121-130.
- Dolinina AYu, Sysoeva MV, van Rijn CM, Sysoev I V. Frequency synchronization reveals that spike-wave discharges in WAG/RIJ rats are significantly nonlinear phenomenon. Journal of Biological Systems. 2024;32(1):239-250 DOI: 10.1142/S0218339024500098.
- Junge L, Parlitz U. Phase synchronization of coupled Ginzburg-Landau equations. Phys Rev E. 2000;62(1):438-441 DOI: 10.1103/PhysRevE.62.438.
- Picovsky A, Rosemblum M, Kurths J. Synchronization: A Universal Concept in Nonlinear Sciences. Cambridge: Cambridge University Press; 2001. 411 p.
- Mormann F, Lehnertz K, David P, Elder C E. Mean phase coherence as a measure for phase synchronization and its application to the EEG of epilepsy patients. Physica D. 2000;144(3-4):358-369 DOI: 10.1016/S0167-2789(00)00087-7.
- Mormann F, Andrzejak RG, Kraskov A, Lehnertz K, Grassberger P. Measuring synchronization in coupled model systems: A comparison of different approaches. Physica D. 2007;225(1):29-42 DOI: 10.1016/J.PHYSD.2006.09.039.
- Nikias CL, Raghuveer M R. Bispectrum estimation: A digital signal processing framework. Proceedings of the IEEE. 1987;75(7):869-891 DOI: 10.1109/PROC.1987.13824.
- Sigl JC, Chamoun N G. An introduction to bispectral analysis for the electroencephalogram. J. Clin. Monitor. Comput. 1994;10:392-404 DOI: 10.1007/BF01618421.
- Basarab МА, Volosyuk VК, Goryachkin ОV, Zelenskii АА, Kravchenko VF, Ksendzuk АV, Kutuza BG, Lukin VV, Trotskii АV, Yakovlev V P. Digital Signal and Image Processing in Radiophysical Applications. М.: Fizmatlit; 2007. 544 p. (in Russian).
- Virtanen P, Gommers R, Oliphant TE, Haberland M, Reddy T, Cournapeau D, Burovski E, Peterson P, Weckesser W, Bright J, van der Walt SJ, Brett M, Wilson J, Millman KJ, Mayorov N, Nelson ARJ, Jones E, Kern R, Larson E, Carey CJ, Polat I, Feng Yu, Moore EW, VanderPlas J, Laxalde D, Perktold J, Cimrman R, Henriksen I, Quintero EA, Harris CR, Archibald AM, Ribeiro AH, Pedregosa F, van Mulbregt P, SciPy 1.0 Contributor s. SciPy 1.0: fundamental algorithms for scientific computing in Python. Nat. Methods. 2020;17:261-272 DOI: 10.1038/s41592-019-0686-2.
- Kramis R, Vanderwolf CH, Bland B H. Two types of hippocampal rhythmical slow activity in both the rabbit and the rat: relations to behavior and effects of atropine, diethyl ether, urethane, and pentobarbital. Exp. Neurol. 1975;49(1):58-85 DOI: 10.1016/0014-4886(75)90195-8.
- Stewart M, Fox S E. Detection of an atropine-resistant component of the hippocampal theta rhythm in urethane-anesthetized rats. Brain Res. 1989;500(1-2):55-60 DOI: 10.1016/0006-8993(89)90299-0.
- Fuhrmann F, Justus D, Sosulina L, Kaneko H, Beutel T, Friedrichs D, Schoch S, Schwarz MK, Fuhrmann M, Remy R. Locomotion, theta oscillations, and the speed-correlated firing of hippocampal neurons are controlled by a medial septal glutamatergic circuit. Neuron. 2015;86(5):1253-1264 DOI: 10.1016/j.neuron.2015.05.001.
- Justus D, Dal"u gge D, Bothe S, Fuhrmann F, Hannes C, Kaneko H, Friedrichs D, Sosulina L, Schwarz I, Elliott DA, Schoch S, Bradke F, Schwarz MK, Remy S. Glutamatergic synaptic integration of locomotion speed via septoentorhinal projections. Nat. Neurosci. 2017;20(1):16-19 DOI: 10.1038/nn.4447.
- Zhou TL, Tamura R, Kuriwaki J, Ono T. Comparison of medial and lateral septal neuron activity during performance of spatial tasks in rats. Hippocampus. 1999;9(3):220-234 DOI: 10.1002/(SICI)1098-1063(1999)9:3<220::AID-HIPO3>3.0.CO;2-E.
- Tsanov M. Speed and oscillations: medial septum integration of attention and navigation. Front. Syst. Neurosci. 2017;11:67 DOI: 10.3389/fnsys.2017.00067.
- Colgin L L. Mechanisms and functions of theta rhythms. Annu. Rev. Neurosci. 2013;36:295-312 DOI: 10.1146/annurev-neuro-062012-170330.
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