Biology:High-frequency oscillations

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Short description: Brainwaves with frequencies larger than 80 Hz
Example of the high-frequency oscillation burst recorded from the brain.

High-frequency oscillations (HFO) are brain waves of the frequency faster than ~80 Hz, generated by neuronal cell population. High-frequency oscillations can be recorded during an electroencephalagram (EEG), local field potential (LFP) or electrocorticogram (ECoG) electrophysiology recordings. They are present in physiological state during sharp waves and ripples - oscillatory patterns involved in memory consolidation processes.[1] HFOs are associated with pathophysiology of the brain like epileptic seizure[2] and are often recorded during seizure onset. It makes a promising biomarker for the identification of the epileptogenic zone.[3][4] Other studies points to the HFO role in psychiatric disorders and possible implications to psychotic episodes in schizophrenia.[5][6][7]

Background and history

Traditional classification of the frequency bands, that are associated to different functions/states of the brain and consist of delta, theta, alpha, beta and gamma bands. Due to the limited capabilities of the early experimental/medical setup to record fast frequencies, for historical reason, all oscillations above 30 Hz were considered as high frequency and were difficult to investigate.[1] Recent advance in manufacturing electrophysiological setups enables to record electric potential with high temporal and space resolution, and to "catch" dynamics of single cell action potential. In neuroscience nomenclature, there is still a reaming gap between ~100 Hz and multi unit activity (>500 Hz), so these oscillations are often called high gamma or HFO.

Neurophysiological features

HFO are generated by different cellular mechanisms and can be detected in many brain areas.[8][9] In hippocampus, this fast neuronal activity is effect of the population synchronous spiking of pyramidal cells in the CA3 region and dendritic layer of the CA1, which give rise to a characteristic oscillation pattern (see more in sharp waves and ripples).[10] The HFO occurrence during memory task (encoding and recalling images) was also reported in human patients from intracranial recordings in primary visual, limbic and higher order cortical areas.[11] Another example of physiological HFO of around 300 Hz, was found in subthalamic nucleus,[12] the brain region which is the main target for high-frequency (130 Hz) deep brain stimulation treatment for patients with Parkinson's disease.  

Somatosensory evoked high-frequency oscillations

ECoG recordings from human somatosensory cortex, has shown HFO (reaching even 600 Hz) presence during sensory evoked potentials and somatosensory evoked magnetic field after median nerve stimulation.[13] These bursts of activity are generated by thalamocortical loop and driven by highly synchronized spiking of the thalamocortical fibres, and are thought to play a role in information processing.[14] Somatosensory evoked HFO amplitude changes may be potentially used as biomarker for neurologic disorders, which can help in diagnosis in certain clinical contexts. Some oncology patients with brain tumors showed higher HFOs amplitude on the same side, where the tumor was. Authors of this study also suggest contribution from the thalamocortical pathways to the fast oscillations.[15] Interestingly, higher HFO amplitudes (between 400 and 800 Hz) after nerve stimulation were also reported in the EEG signal of healthy football and racquet sports players.[16]

Pathological HFO

There are many studies, that reports pathophysiological types of HFO in human patients and animal models of disease, which are related to different psychiatric or neurological disorders:

  • Amplitude aberrations of the sensory evoked HFOs (600 Hz) was reported in mild demyelination in multiple sclerosis patients.[17]
  • HFO (>80 Hz) occur during epileptic seizure onset.[18][19]
  • Disruption in the HFO (200–500 Hz) synchronization in subthalamic nucleus is related to Parkinson's disease symptoms.[20][12]
  • HFOs are visible in different brain regions just after cardiac-arrest and are linked to near-death states.[21]
  • High amplitude HFOs (80–200 Hz) bursts correlates with psychotic-like state evoked with PCP or subanesthetic dose of ketamine (and other NMDA receptor blockers).[6][22][23]

NMDA receptor hypofunction HFO

Current source density reconstruction (done with kCSD method,[24] red and blue dots) of the example HFO burst recorded (6 channel setup - green dots) from rat's brain (grey dots).

There are increasing number of studies indicating that HFO rhythms (130–180 Hz) may arise due to the local NMDA receptor blockage,[25][26][27][28] which is also a pharmacological model of schizophrenia.[26] These NMDA receptor dependent fast oscillations were detected in different brain areas including hippocampus,[29] nucleus accumbens[6] and prefrontal cortex regions.[30] Despite the fact that this type of HFO was not yet confirmed in human patients, second generation antipsychotic drugs, widely used to treat schizophrenia and schizoaffective disorders (i.e. Clozapine, Risperidone), were shown to reduce HFO frequency.[6] Recent studies, reports on the new source of HFO in the olfactory bulb structures, which is surprisingly stronger than any other previously seen in the mammalian brain.[31][32] HFO in the bulb is generated by local excitatory-inhibitory circuits modulated by breathing rhythm and may be also recorded under ketamine-xylazine anesthesia.[33] This findings may aid understanding early symptoms of schizophrenia patients and their relatives, that can suffer from olfactory system impairments.[34]

See also

Brain waves

References

  1. ↑ 1.0 1.1 Buzsáki, György; da Silva, Fernando Lopes (September 2012). "High frequency oscillations in the intact brain". Progress in Neurobiology 98 (3): 241–249. doi:10.1016/j.pneurobio.2012.02.004. ISSN 0301-0082. PMID 22449727. 
  2. ↑ Engel, Jerome; Bragin, Anatol; Staba, Richard; Mody, Istvan (April 2009). "High-frequency oscillations: what is normal and what is not?". Epilepsia 50 (4): 598–604. doi:10.1111/j.1528-1167.2008.01917.x. ISSN 1528-1167. PMID 19055491. 
  3. ↑ Jacobs, J.; Staba, R.; Asano, E.; Otsubo, H.; Wu, J.Y.; Zijlmans, M.; Mohamed, I.; Kahane, P. et al. (September 2012). "High-frequency oscillations (HFOs) in clinical epilepsy". Progress in Neurobiology 98 (3): 302–315. doi:10.1016/j.pneurobio.2012.03.001. ISSN 0301-0082. PMID 22480752. 
  4. ↑ Arroyo, Santiago; Uematsu, Sumio (July 1992). "High-Frequency EEG Activity at the Start of Seizures" (in en). Journal of Clinical Neurophysiology 9 (3): 441–448. doi:10.1097/00004691-199207010-00012. ISSN 0736-0258. PMID 1517412. https://dx.doi.org/10.1097%2F00004691-199207010-00012. 
  5. ↑ Uhlhaas, Peter J.; Singer, Wolf (September 2013). "High-frequency oscillations and the neurobiology of schizophrenia". Dialogues in Clinical Neuroscience 15 (3): 301–313. doi:10.31887/DCNS.2013.15.3/puhlhaas. ISSN 1294-8322. PMID 24174902. 
  6. ↑ 6.0 6.1 6.2 6.3 Olszewski, Maciej; Piasecka, Joanna; Goda, Sailaja A.; Kasicki, Stefan; Hunt, Mark J. (June 2013). "Antipsychotic compounds differentially modulate high-frequency oscillations in the rat nucleus accumbens: a comparison of first- and second-generation drugs". The International Journal of Neuropsychopharmacology 16 (5): 1009–1020. doi:10.1017/S1461145712001034. ISSN 1469-5111. PMID 23171738. 
  7. ↑ Goda, Sailaja A.; Olszewski, Maciej; Piasecka, Joanna; Rejniak, Karolina; Whittington, Miles A.; Kasicki, Stefan; Hunt, Mark J. (August 2015). "Aberrant high frequency oscillations recorded in the rat nucleus accumbens in the methylazoxymethanol acetate neurodevelopmental model of schizophrenia". Progress in Neuro-Psychopharmacology and Biological Psychiatry 61: 44–51. doi:10.1016/j.pnpbp.2015.03.016. ISSN 0278-5846. PMID 25862088. http://dx.doi.org/10.1016/j.pnpbp.2015.03.016. 
  8. ↑ Haufler, Darrell; Pare, Denis (2014-07-01). "High-frequency oscillations are prominent in the extended amygdala". Journal of Neurophysiology 112 (1): 110–119. doi:10.1152/jn.00107.2014. ISSN 0022-3077. PMID 24717353. 
  9. ↑ Zhong, Weiwei; Ciatipis, Mareva; Wolfenstetter, Thérèse; Jessberger, Jakob; Müller, Carola; Ponsel, Simon; Yanovsky, Yevgenij; Brankačk, Jurij et al. (2017-04-25). "Selective entrainment of gamma subbands by different slow network oscillations". Proceedings of the National Academy of Sciences of the United States of America 114 (17): 4519–4524. doi:10.1073/pnas.1617249114. ISSN 0027-8424. PMID 28396398. 
  10. ↑ Ylinen, A.; Bragin, A.; Nádasdy, Z.; Jandó, G.; Szabó, I.; Sik, A.; Buzsáki, G. (January 1995). "Sharp wave-associated high-frequency oscillation (200 Hz) in the intact hippocampus: network and intracellular mechanisms". The Journal of Neuroscience 15 (1 Pt 1): 30–46. doi:10.1523/JNEUROSCI.15-01-00030.1995. ISSN 0270-6474. PMID 7823136. 
  11. ↑ Kucewicz, Michal T.; Cimbalnik, Jan; Matsumoto, Joseph Y.; Brinkmann, Benjamin H.; Bower, Mark R.; Vasoli, Vincent; Sulc, Vlastimil; Meyer, Fred et al. (August 2014). "High frequency oscillations are associated with cognitive processing in human recognition memory". Brain 137 (8): 2231–2244. doi:10.1093/brain/awu149. ISSN 0006-8950. PMID 24919972. 
  12. ↑ 12.0 12.1 Foffani, G. (2003-06-23). "300-Hz subthalamic oscillations in Parkinson's disease" (in en). Brain 126 (10): 2153–2163. doi:10.1093/brain/awg229. ISSN 1460-2156. PMID 12937087. 
  13. ↑ Burnos, Sergey; Fedele, Tommaso; Schmid, Olivier; Krayenbühl, Niklaus; Sarnthein, Johannes (2016-01-01). "Detectability of the somatosensory evoked high frequency oscillation (HFO) co-recorded by scalp EEG and ECoG under propofol" (in en). NeuroImage: Clinical 10: 318–325. doi:10.1016/j.nicl.2015.11.018. ISSN 2213-1582. PMID 26900572. 
  14. ↑ Ozaki, Isamu; Hashimoto, Isao (2011-10-01). "Exploring the physiology and function of high-frequency oscillations (HFOs) from the somatosensory cortex" (in en). Clinical Neurophysiology 122 (10): 1908–1923. doi:10.1016/j.clinph.2011.05.023. ISSN 1388-2457. PMID 21724458. http://www.sciencedirect.com/science/article/pii/S1388245711003750. 
  15. ↑ Ooba, Hiroshi; Abe, Tatsuya; Kamida, Tohru; Anan, Mitsuhiro; Morishige, Masaki; Fujiki, Minoru (April 2010). "Increasing high-frequency oscillations (HFOs) in patients with brain tumours: implication for increasing amplitude of N20". Clinical Neurophysiology 121 (4): 474–481. doi:10.1016/j.clinph.2009.12.007. ISSN 1872-8952. PMID 20097127. https://pubmed.ncbi.nlm.nih.gov/20097127/. 
  16. ↑ Murakami, Takenobu; Sakuma, Kenji; Nakashima, Kenji (2008-12-01). "Somatosensory evoked potentials and high-frequency oscillations in athletes" (in en). Clinical Neurophysiology 119 (12): 2862–2869. doi:10.1016/j.clinph.2008.09.002. ISSN 1388-2457. PMID 18849191. http://www.sciencedirect.com/science/article/pii/S138824570800936X. 
  17. ↑ Gobbelé, René; Waberski, Till Dino; Dieckhöfer, Anne; Kawohl, Wolfram; Klostermann, Fabian; Curio, Gabriel; Buchner, Helmut (July 2003). "Patterns of disturbed impulse propagation in multiple sclerosis identified by low and high frequency somatosensory evoked potential components". Journal of Clinical Neurophysiology 20 (4): 283–290. doi:10.1097/00004691-200307000-00008. ISSN 0736-0258. PMID 14530742. https://pubmed.ncbi.nlm.nih.gov/14530742/. 
  18. ↑ Zijlmans, Maeike; Jiruska, Premysl; Zelmann, Rina; Leijten, Frans S. S.; Jefferys, John G. R.; Gotman, Jean (February 2012). "High-frequency oscillations as a new biomarker in epilepsy". Annals of Neurology 71 (2): 169–178. doi:10.1002/ana.22548. ISSN 1531-8249. PMID 22367988. 
  19. ↑ Frauscher, Birgit; Bartolomei, Fabrice; Kobayashi, Katsuhiro; Cimbalnik, Jan; van't Klooster, Maryse A.; Rampp, Stefan; Otsubo, Hiroshi; Höller, Yvonne et al. (August 2017). "High-frequency oscillations: The state of clinical research". Epilepsia 58 (8): 1316–1329. doi:10.1111/epi.13829. ISSN 0013-9580. PMID 28666056. 
  20. ↑ Yang, Andrew I.; Vanegas, Nora; Lungu, Codrin; Zaghloul, Kareem A. (2014-09-17). "Beta-coupled high-frequency activity and beta-locked neuronal spiking in the subthalamic nucleus of Parkinson's disease". The Journal of Neuroscience 34 (38): 12816–12827. doi:10.1523/JNEUROSCI.1895-14.2014. ISSN 1529-2401. PMID 25232117. 
  21. ↑ Borjigin, Jimo; Lee, UnCheol; Liu, Tiecheng; Pal, Dinesh; Huff, Sean; Klarr, Daniel; Sloboda, Jennifer; Hernandez, Jason et al. (2013-08-27). "Surge of neurophysiological coherence and connectivity in the dying brain". Proceedings of the National Academy of Sciences of the United States of America 110 (35): 14432–14437. doi:10.1073/pnas.1308285110. ISSN 1091-6490. PMID 23940340. Bibcode: 2013PNAS..11014432B. 
  22. ↑ Hunt, Mark J.; Olszewski, Maciej; Piasecka, Joanna; Whittington, Miles A.; Kasicki, Stefan (2015). "Effects of NMDA receptor antagonists and antipsychotics on high frequency oscillations recorded in the nucleus accumbens of freely moving mice". Psychopharmacology 232 (24): 4525–4535. doi:10.1007/s00213-015-4073-0. ISSN 0033-3158. PMID 26446869. 
  23. ↑ Hunt, Mark J; Kasicki, Stefan (2013-07-17). "A systematic review of the effects of NMDA receptor antagonists on oscillatory activity recorded in vivo". Journal of Psychopharmacology 27 (11): 972–986. doi:10.1177/0269881113495117. ISSN 0269-8811. PMID 23863924. http://dx.doi.org/10.1177/0269881113495117. 
  24. ↑ Chintaluri, Chaitanya; Bejtka, Marta; Średniawa, Władysław; Czerwiński, Michał; Dzik, Jakub M.; Jędrzejewska-Szmek, Joanna; Kondrakiewicz, Kacper; Kublik, Ewa et al. (2021-05-14). "What we can and what we cannot see with extracellular multielectrodes" (in en). PLOS Computational Biology 17 (5): e1008615. doi:10.1371/journal.pcbi.1008615. ISSN 1553-7358. PMID 33989280. Bibcode: 2021PLSCB..17E8615C. 
  25. ↑ Hunt, Mark Jeremy; Raynaud, Beryl; Garcia, Rene (2006-12-01). "Ketamine dose-dependently induces high-frequency oscillations in the nucleus accumbens in freely moving rats". Biological Psychiatry 60 (11): 1206–1214. doi:10.1016/j.biopsych.2006.01.020. ISSN 0006-3223. PMID 16650831. https://pubmed.ncbi.nlm.nih.gov/16650831/. 
  26. ↑ 26.0 26.1 Frohlich, Joel; Van Horn, John D. (April 2014). "Reviewing the ketamine model for schizophrenia". Journal of Psychopharmacology 28 (4): 287–302. doi:10.1177/0269881113512909. ISSN 1461-7285. PMID 24257811. 
  27. ↑ Phillips, K.G.; Cotel, M.C.; McCarthy, A.P.; Edgar, D.M.; Tricklebank, M.; O'Neill, M.J.; Jones, M.W.; Wafford, K.A. (March 2012). "Differential effects of NMDA antagonists on high frequency and gamma EEG oscillations in a neurodevelopmental model of schizophrenia" (in en). Neuropharmacology 62 (3): 1359–1370. doi:10.1016/j.neuropharm.2011.04.006. PMID 21521646. https://linkinghub.elsevier.com/retrieve/pii/S0028390811001511. 
  28. ↑ Hansen, Ingeborg H.; Agerskov, Claus; Arvastson, Lars; Bastlund, Jesper F.; Sørensen, Helge B. D.; Herrik, Kjartan F. (July 2019). "Pharmaco-electroencephalographic responses in the rat differ between active and inactive locomotor states". The European Journal of Neuroscience 50 (2): 1948–1971. doi:10.1111/ejn.14373. ISSN 1460-9568. PMID 30762918. 
  29. ↑ Caixeta, Fábio V.; Cornélio, Alianda M.; Scheffer-Teixeira, Robson; Ribeiro, Sidarta; Tort, Adriano B. L. (2013-08-02). "Ketamine alters oscillatory coupling in the hippocampus". Scientific Reports 3: 2348. doi:10.1038/srep02348. ISSN 2045-2322. PMID 23907109. Bibcode: 2013NatSR...3E2348C. 
  30. ↑ Pittman-Polletta, Benjamin; Hu, Kun; Kocsis, Bernat (2018-08-02). "Subunit-specific NMDAR antagonism dissociates schizophrenia subtype-relevant oscillopathies associated with frontal hypofunction and hippocampal hyperfunction". Scientific Reports 8 (1): 11588. doi:10.1038/s41598-018-29331-8. ISSN 2045-2322. PMID 30072757. Bibcode: 2018NatSR...811588P. 
  31. ↑ Hunt, Mark Jeremy; Adams, Natalie E.; Średniawa, Władysław; Wójcik, Daniel K.; Simon, Anna; Kasicki, Stefan; Whittington, Miles Adrian (January 2019). "The olfactory bulb is a source of high-frequency oscillations (130–180 Hz) associated with a subanesthetic dose of ketamine in rodents" (in en). Neuropsychopharmacology 44 (2): 435–442. doi:10.1038/s41386-018-0173-y. ISSN 1740-634X. PMID 30140046. 
  32. ↑ Wróbel, Jacek; Średniawa, Władysław; Jurkiewicz, Gabriela; Żygierewicz, Jarosław; Wójcik, Daniel K.; Whittington, Miles Adrian; Hunt, Mark Jeremy (2020-11-04). "Nasal respiration is necessary for ketamine-dependent high frequency network oscillations and behavioral hyperactivity in rats" (in en). Scientific Reports 10 (1): 18981. doi:10.1038/s41598-020-75641-1. ISSN 2045-2322. PMID 33149202. Bibcode: 2020NatSR..1018981W. 
  33. ↑ Średniawa, Władysław; Wróbel, Jacek; Kublik, Ewa; Wójcik, Daniel Krzysztof; Whittington, Miles Adrian; Hunt, Mark Jeremy (2021-03-18). "Network and synaptic mechanisms underlying high frequency oscillations in the rat and cat olfactory bulb under ketamine-xylazine anesthesia" (in en). Scientific Reports 11 (1): 6390. doi:10.1038/s41598-021-85705-5. ISSN 2045-2322. PMID 33737621. 
  34. ↑ Turetsky, Bruce I; Hahn, Chang-Gyu; Arnold, Steven E; Moberg, Paul J (February 2009). "Olfactory Receptor Neuron Dysfunction in Schizophrenia". Neuropsychopharmacology 34 (3): 767–774. doi:10.1038/npp.2008.139. ISSN 0893-133X. PMID 18754006. 



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