High-frequency oscillations

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Example of the high-frequency oscillation burst recorded from the brain. HFO wiki.jpg
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]

Contents

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:

NMDA receptor hypofunction HFO

Current source density reconstruction (done with kCSD method, red and blue dots) of the example HFO burst recorded (6 channel setup - green dots) from rat's brain (grey dots). Hfo rat.gif
Current source density reconstruction (done with kCSD method, 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 2 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. PMC   4895831 . 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. S2CID   18528403.
  3. ↑ Jacobs, J.; Staba, R.; Asano, E.; Otsubo, H.; Wu, J.Y.; Zijlmans, M.; Mohamed, I.; Kahane, P.; Dubeau, F.; Navarro, V.; Gotman, J. (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. PMC   3674884 . PMID   22480752.
  4. ↑ Arroyo, Santiago; Uematsu, Sumio (July 1992). "High-Frequency EEG Activity at the Start of Seizures" . Journal of Clinical Neurophysiology. 9 (3): 441–448. doi:10.1097/00004691-199207010-00012. ISSN   0736-0258. PMID   1517412.
  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. PMC   3811102 . PMID   24174902.
  6. 1 2 3 4 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. S2CID   13965042.
  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. PMC   4064387 . PMID   24717353.
  9. ↑ Zhong, Weiwei; Ciatipis, Mareva; Wolfenstetter, Thérèse; Jessberger, Jakob; Müller, Carola; Ponsel, Simon; Yanovsky, Yevgenij; Brankačk, Jurij; Tort, Adriano B. L.; Draguhn, Andreas (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. Bibcode:2017PNAS..114.4519Z. doi: 10.1073/pnas.1617249114 . ISSN   0027-8424. PMC   5410835 . 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. PMC   6578299 . PMID   7823136.
  11. ↑ Kucewicz, Michal T.; Cimbalnik, Jan; Matsumoto, Joseph Y.; Brinkmann, Benjamin H.; Bower, Mark R.; Vasoli, Vincent; Sulc, Vlastimil; Meyer, Fred; Marsh, W. R.; Stead, S. M.; Worrell, Gregory A. (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. PMC   4107742 . PMID   24919972.
  12. 1 2 Foffani, G. (2003-06-23). "300-Hz subthalamic oscillations in Parkinson's disease". 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". NeuroImage: Clinical. 10: 318–325. doi:10.1016/j.nicl.2015.11.018. ISSN   2213-1582. PMC   4723731 . PMID   26900572.
  14. ↑ Ozaki, Isamu; Hashimoto, Isao (2011-10-01). "Exploring the physiology and function of high-frequency oscillations (HFOs) from the somatosensory cortex" . Clinical Neurophysiology. 122 (10): 1908–1923. doi:10.1016/j.clinph.2011.05.023. ISSN   1388-2457. PMID   21724458. S2CID   7628474.
  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. S2CID   206793052.
  16. ↑ Murakami, Takenobu; Sakuma, Kenji; Nakashima, Kenji (2008-12-01). "Somatosensory evoked potentials and high-frequency oscillations in athletes" . Clinical Neurophysiology. 119 (12): 2862–2869. doi:10.1016/j.clinph.2008.09.002. ISSN   1388-2457. PMID   18849191. S2CID   30129908.
  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. S2CID   24099633.
  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. PMC   3754947 . PMID   22367988.
  19. ↑ Frauscher, Birgit; Bartolomei, Fabrice; Kobayashi, Katsuhiro; Cimbalnik, Jan; van't Klooster, Maryse A.; Rampp, Stefan; Otsubo, Hiroshi; Höller, Yvonne; Wu, Joyce Y.; Asano, Eishi; Engel, Jerome (August 2017). "High-frequency oscillations: The state of clinical research". Epilepsia. 58 (8): 1316–1329. doi:10.1111/epi.13829. ISSN   0013-9580. PMC   5806699 . 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. PMC   4166162 . PMID   25232117.
  21. ↑ Borjigin, Jimo; Lee, UnCheol; Liu, Tiecheng; Pal, Dinesh; Huff, Sean; Klarr, Daniel; Sloboda, Jennifer; Hernandez, Jason; Wang, Michael M.; Mashour, George A. (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. Bibcode:2013PNAS..11014432B. doi: 10.1073/pnas.1308285110 . ISSN   1091-6490. PMC   3761619 . PMID   23940340.
  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. PMC   4646921 . 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. S2CID   31344362.
  24. ↑ Chintaluri, Chaitanya; Bejtka, Marta; Średniawa, Władysław; Czerwiński, Michał; Dzik, Jakub M.; Jędrzejewska-Szmek, Joanna; Kondrakiewicz, Kacper; Kublik, Ewa; Wójcik, Daniel K. (2021-05-14). "What we can and what we cannot see with extracellular multielectrodes". PLOS Computational Biology. 17 (5): e1008615. Bibcode:2021PLSCB..17E8615C. doi: 10.1371/journal.pcbi.1008615 . ISSN   1553-7358. PMC   8153483 . PMID   33989280.
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  26. 1 2 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. PMC   4133098 . 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" . Neuropharmacology. 62 (3): 1359–1370. doi:10.1016/j.neuropharm.2011.04.006. PMID   21521646. S2CID   23058003.
  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. PMC   6806018 . 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. Bibcode:2013NatSR...3.2348C. doi:10.1038/srep02348. ISSN   2045-2322. PMC   3731648 . PMID   23907109.
  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. Bibcode:2018NatSR...811588P. doi:10.1038/s41598-018-29331-8. ISSN   2045-2322. PMC   6072790 . PMID   30072757.
  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". Neuropsychopharmacology. 44 (2): 435–442. doi: 10.1038/s41386-018-0173-y . ISSN   1740-634X. PMC   6300534 . 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". Scientific Reports. 10 (1): 18981. Bibcode:2020NatSR..1018981W. doi: 10.1038/s41598-020-75641-1 . ISSN   2045-2322. PMC   7642442 . PMID   33149202.
  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". Scientific Reports. 11 (1): 6390. doi: 10.1038/s41598-021-85705-5 . ISSN   2045-2322. PMC   7973548 . 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. PMC   3524971 . PMID   18754006.
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