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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].

Background and history

[edit]

Classical classification of the frequency bands, that are associated to different functions/states of the brain 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 even 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

[edit]

HFO are generated by different cellular mechanisms and can be detected in many brain areas [7][8]. 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) [9]. 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 [10]. Another example of physiological HFO of around 300 Hz, was found in subthalamic nucleus [11], which partially explains, why high frequency deep brain stimulation treatment helps patients with Parkinson's disease.

Somatosensory evoked high-frequency oscillations

[edit]

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[12]. 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 [13]. 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[14]. Interestingly, higher HFO amplitudes (between 400–800 Hz) after nerve stimulation were also reported in the EEG signal of healthy football and racquet sports players[15].

Pathological HFO

[edit]

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

[edit]
Current source density reconstruction (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 [22][23][24][25], which is also a pharmacological model of schizophrenia [23]. These NMDA receptor dependent fast oscillations were detected in different brain areas including hippocampus [26], nucleus accumbens [6] and prefrontal cortex regions [27]. Despite the fact, that these 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), was 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 [28]. This findings may help to explain early symptoms of schizophrenia patients, that suffer from olfactory system impairments [29].

References

[edit]

High frequency oscillations (HFO)

[edit]
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 [30] and are often recorded during seizure onset. It makes a promising biomarker for the identification of the epileptogenic zone [31][32]. Other studies points to the HFO role in psychiatric disorders and possible implications to psychotic episodes in schizophrenia [33][6].

Background and history

[edit]

Classical classification of the frequency bands, that are associated to different functions/states of the brain 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 even 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

[edit]

HFO are generated by different cellular mechanisms and can be detected in many brain areas [34][35]. 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) [36]. 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 [37]. Another example of physiological HFO of around 300 Hz, was found in subthalamic nucleus [38], which partially explains, why high frequency deep brain stimulation treatment helps patients with Parkinson's disease.

Somatosensory evoked high-frequency oscillations

[edit]

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[39]. 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 [40]. 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[41]. Interestingly, higher HFO amplitudes (between 400–800 Hz) after nerve stimulation were also reported in the EEG signal of healthy football and racquet sports players[42].

Pathological HFO

[edit]

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

[edit]
Current source density reconstruction (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 [49][23][50][51], which is also a pharmacological model of schizophrenia [23]. These NMDA receptor dependent fast oscillations were detected in different brain areas including hippocampus [52], nucleus accumbens [6] and prefrontal cortex regions [53]. Despite the fact, that these 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), was 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 [54]. This findings may help to explain early symptoms of schizophrenia patients, that suffer from olfactory system impairments [55].

References

[edit]
  1. ^ a b c d Buzsáki, György; da Silva, Fernando Lopes (2012-9). "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. {{cite journal}}: Check date values in: |date= (help)
  2. ^ Engel, Jerome; Bragin, Anatol; Staba, Richard; Mody, Istvan (2009-04). "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. {{cite journal}}: Check date values in: |date= (help)
  3. ^ Jacobs, J.; Staba, R.; Asano, E.; Otsubo, H.; Wu, J.Y.; Zijlmans, M.; Mohamed, I.; Kahane, P.; Dubeau, F.; Navarro, V.; Gotman, J. (2012-9). "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. {{cite journal}}: Check date values in: |date= (help)
  4. ^ Arroyo, Santiago; Uematsu, Sumio (1992-07). "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. {{cite journal}}: Check date values in: |date= (help)
  5. ^ Uhlhaas, Peter J.; Singer, Wolf (2013-9). "High-frequency oscillations and the neurobiology of schizophrenia". Dialogues in Clinical Neuroscience. 15 (3): 301–313. ISSN 1294-8322. PMC 3811102. PMID 24174902. {{cite journal}}: Check date values in: |date= (help)
  6. ^ a b c d e f g h Olszewski, Maciej; Piasecka, Joanna; Goda, Sailaja A.; Kasicki, Stefan; Hunt, Mark J. (2013-06). "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. {{cite journal}}: Check date values in: |date= (help)
  7. ^ 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.
  8. ^ 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. doi:10.1073/pnas.1617249114. ISSN 0027-8424. PMC 5410835. PMID 28396398.
  9. ^ Ylinen, A.; Bragin, A.; Nádasdy, Z.; Jandó, G.; Szabó, I.; Sik, A.; Buzsáki, G. (1995-01). "Sharp wave-associated high-frequency oscillation (200 Hz) in the intact hippocampus: network and intracellular mechanisms". The Journal of Neuroscience: The Official Journal of the Society for Neuroscience. 15 (1 Pt 1): 30–46. doi:10.1523/JNEUROSCI.15-01-00030.1995. ISSN 0270-6474. PMC 6578299. PMID 7823136. {{cite journal}}: Check date values in: |date= (help)
  10. ^ 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. (2014-8). "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. {{cite journal}}: Check date values in: |date= (help)
  11. ^ 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.
  12. ^ 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.
  13. ^ 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.
  14. ^ Ooba, Hiroshi; Abe, Tatsuya; Kamida, Tohru; Anan, Mitsuhiro; Morishige, Masaki; Fujiki, Minoru (2010-04). "Increasing high-frequency oscillations (HFOs) in patients with brain tumours: implication for increasing amplitude of N20". Clinical Neurophysiology: Official Journal of the International Federation of Clinical Neurophysiology. 121 (4): 474–481. doi:10.1016/j.clinph.2009.12.007. ISSN 1872-8952. PMID 20097127. {{cite journal}}: Check date values in: |date= (help)
  15. ^ 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.
  16. ^ Gobbelé, René; Waberski, Till Dino; Dieckhöfer, Anne; Kawohl, Wolfram; Klostermann, Fabian; Curio, Gabriel; Buchner, Helmut (2003-07). "Patterns of disturbed impulse propagation in multiple sclerosis identified by low and high frequency somatosensory evoked potential components". Journal of Clinical Neurophysiology: Official Publication of the American Electroencephalographic Society. 20 (4): 283–290. doi:10.1097/00004691-200307000-00008. ISSN 0736-0258. PMID 14530742. {{cite journal}}: Check date values in: |date= (help)
  17. ^ Zijlmans, Maeike; Jiruska, Premysl; Zelmann, Rina; Leijten, Frans S. S.; Jefferys, John G. R.; Gotman, Jean (2012-02). "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. {{cite journal}}: Check date values in: |date= (help)
  18. ^ 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 (2017-8). "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. {{cite journal}}: Check date values in: |date= (help)
  19. ^ 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: The Official Journal of the Society for Neuroscience. 34 (38): 12816–12827. doi:10.1523/JNEUROSCI.1895-14.2014. ISSN 1529-2401. PMC 4166162. PMID 25232117.
  20. ^ 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.
  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. doi:10.1073/pnas.1308285110. ISSN 1091-6490. PMC 3761619. PMID 23940340.
  22. ^ 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.
  23. ^ a b c d Frohlich, Joel; Van Horn, John D. (2014-04). "Reviewing the ketamine model for schizophrenia". Journal of Psychopharmacology (Oxford, England). 28 (4): 287–302. doi:10.1177/0269881113512909. ISSN 1461-7285. PMC 4133098. PMID 24257811. {{cite journal}}: Check date values in: |date= (help)
  24. ^ Phillips, K.G.; Cotel, M.C.; McCarthy, A.P.; Edgar, D.M.; Tricklebank, M.; O’Neill, M.J.; Jones, M.W.; Wafford, K.A. (2012-03). "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. {{cite journal}}: Check date values in: |date= (help)
  25. ^ Hansen, Ingeborg H.; Agerskov, Claus; Arvastson, Lars; Bastlund, Jesper F.; Sørensen, Helge B. D.; Herrik, Kjartan F. (07 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. {{cite journal}}: Check date values in: |date= (help)
  26. ^ 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. doi:10.1038/srep02348. ISSN 2045-2322. PMC 3731648. PMID 23907109.
  27. ^ 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. doi:10.1038/s41598-018-29331-8. ISSN 2045-2322. PMC 6072790. PMID 30072757.
  28. ^ Hunt, Mark Jeremy; Adams, Natalie E.; Średniawa, Władysław; Wójcik, Daniel K.; Simon, Anna; Kasicki, Stefan; Whittington, Miles Adrian (01 2019). "The olfactory bulb is a source of high-frequency oscillations (130-180 Hz) associated with a subanesthetic dose of ketamine in rodents". Neuropsychopharmacology: Official Publication of the American College of Neuropsychopharmacology. 44 (2): 435–442. doi:10.1038/s41386-018-0173-y. ISSN 1740-634X. PMC 6300534. PMID 30140046. {{cite journal}}: Check date values in: |date= (help)
  29. ^ Turetsky, Bruce I; Hahn, Chang-Gyu; Arnold, Steven E; Moberg, Paul J (2009-2). "Olfactory Receptor Neuron Dysfunction in Schizophrenia". Neuropsychopharmacology : official publication of the American College of Neuropsychopharmacology. 34 (3): 767–774. doi:10.1038/npp.2008.139. ISSN 0893-133X. PMC 3524971. PMID 18754006. {{cite journal}}: Check date values in: |date= (help)
  30. ^ Engel, Jerome; Bragin, Anatol; Staba, Richard; Mody, Istvan (2009-04). "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. {{cite journal}}: Check date values in: |date= (help)
  31. ^ Jacobs, J.; Staba, R.; Asano, E.; Otsubo, H.; Wu, J.Y.; Zijlmans, M.; Mohamed, I.; Kahane, P.; Dubeau, F.; Navarro, V.; Gotman, J. (2012-9). "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. {{cite journal}}: Check date values in: |date= (help)
  32. ^ Arroyo, Santiago; Uematsu, Sumio (1992-07). "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. {{cite journal}}: Check date values in: |date= (help)
  33. ^ Uhlhaas, Peter J.; Singer, Wolf (2013-9). "High-frequency oscillations and the neurobiology of schizophrenia". Dialogues in Clinical Neuroscience. 15 (3): 301–313. ISSN 1294-8322. PMC 3811102. PMID 24174902. {{cite journal}}: Check date values in: |date= (help)
  34. ^ 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.
  35. ^ 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. doi:10.1073/pnas.1617249114. ISSN 0027-8424. PMC 5410835. PMID 28396398.
  36. ^ Ylinen, A.; Bragin, A.; Nádasdy, Z.; Jandó, G.; Szabó, I.; Sik, A.; Buzsáki, G. (1995-01). "Sharp wave-associated high-frequency oscillation (200 Hz) in the intact hippocampus: network and intracellular mechanisms". The Journal of Neuroscience: The Official Journal of the Society for Neuroscience. 15 (1 Pt 1): 30–46. doi:10.1523/JNEUROSCI.15-01-00030.1995. ISSN 0270-6474. PMC 6578299. PMID 7823136. {{cite journal}}: Check date values in: |date= (help)
  37. ^ 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. (2014-8). "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. {{cite journal}}: Check date values in: |date= (help)
  38. ^ 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.
  39. ^ 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.
  40. ^ 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.
  41. ^ Ooba, Hiroshi; Abe, Tatsuya; Kamida, Tohru; Anan, Mitsuhiro; Morishige, Masaki; Fujiki, Minoru (2010-04). "Increasing high-frequency oscillations (HFOs) in patients with brain tumours: implication for increasing amplitude of N20". Clinical Neurophysiology: Official Journal of the International Federation of Clinical Neurophysiology. 121 (4): 474–481. doi:10.1016/j.clinph.2009.12.007. ISSN 1872-8952. PMID 20097127. {{cite journal}}: Check date values in: |date= (help)
  42. ^ 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.
  43. ^ Gobbelé, René; Waberski, Till Dino; Dieckhöfer, Anne; Kawohl, Wolfram; Klostermann, Fabian; Curio, Gabriel; Buchner, Helmut (2003-07). "Patterns of disturbed impulse propagation in multiple sclerosis identified by low and high frequency somatosensory evoked potential components". Journal of Clinical Neurophysiology: Official Publication of the American Electroencephalographic Society. 20 (4): 283–290. doi:10.1097/00004691-200307000-00008. ISSN 0736-0258. PMID 14530742. {{cite journal}}: Check date values in: |date= (help)
  44. ^ Zijlmans, Maeike; Jiruska, Premysl; Zelmann, Rina; Leijten, Frans S. S.; Jefferys, John G. R.; Gotman, Jean (2012-02). "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. {{cite journal}}: Check date values in: |date= (help)
  45. ^ 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 (2017-8). "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. {{cite journal}}: Check date values in: |date= (help)
  46. ^ 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: The Official Journal of the Society for Neuroscience. 34 (38): 12816–12827. doi:10.1523/JNEUROSCI.1895-14.2014. ISSN 1529-2401. PMC 4166162. PMID 25232117.
  47. ^ 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.
  48. ^ 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. doi:10.1073/pnas.1308285110. ISSN 1091-6490. PMC 3761619. PMID 23940340.
  49. ^ 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.
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