High-frequency oscillations
{{Short description|Brainwaves with frequencies larger than 80 Hz}}
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.{{Cite journal|last1=Buzsáki|first1=György|last2=da Silva|first2=Fernando Lopes|date=September 2012|title=High frequency oscillations in the intact brain|journal=Progress in Neurobiology|volume=98|issue=3|pages=241–249|doi=10.1016/j.pneurobio.2012.02.004|issn=0301-0082|pmc=4895831|pmid=22449727}} HFOs are associated with pathophysiology of the brain like epileptic seizure{{Cite journal|last1=Engel|first1=Jerome|last2=Bragin|first2=Anatol|last3=Staba|first3=Richard|last4=Mody|first4=Istvan|date=April 2009|title=High-frequency oscillations: what is normal and what is not?|journal=Epilepsia|volume=50|issue=4|pages=598–604|doi=10.1111/j.1528-1167.2008.01917.x|issn=1528-1167|pmid=19055491|s2cid=18528403|doi-access=free}} and are often recorded during seizure onset. It makes a promising biomarker for the identification of the epileptogenic zone.{{Cite journal|last1=Jacobs|first1=J.|last2=Staba|first2=R.|last3=Asano|first3=E.|last4=Otsubo|first4=H.|last5=Wu|first5=J.Y.|last6=Zijlmans|first6=M.|last7=Mohamed|first7=I.|last8=Kahane|first8=P.|last9=Dubeau|first9=F.|last10=Navarro|first10=V.|last11=Gotman|first11=J.|date=September 2012|title=High-frequency oscillations (HFOs) in clinical epilepsy|journal=Progress in Neurobiology|volume=98|issue=3|pages=302–315|doi=10.1016/j.pneurobio.2012.03.001|issn=0301-0082|pmc=3674884|pmid=22480752}}{{Cite journal|last1=Arroyo|first1=Santiago|last2=Uematsu|first2=Sumio|date=July 1992|title=High-Frequency EEG Activity at the Start of Seizures|url=https://dx.doi.org/10.1097%2F00004691-199207010-00012|journal=Journal of Clinical Neurophysiology|language=en|volume=9|issue=3|pages=441–448|doi=10.1097/00004691-199207010-00012|pmid=1517412|issn=0736-0258}} Other studies points to the HFO role in psychiatric disorders and possible implications to psychotic episodes in schizophrenia.{{Cite journal|last1=Uhlhaas|first1=Peter J.|last2=Singer|first2=Wolf|date=September 2013|title=High-frequency oscillations and the neurobiology of schizophrenia|journal=Dialogues in Clinical Neuroscience|volume=15|issue=3|pages=301–313|doi=10.31887/DCNS.2013.15.3/puhlhaas|issn=1294-8322|pmc=3811102|pmid=24174902}}{{Cite journal|last1=Olszewski|first1=Maciej|last2=Piasecka|first2=Joanna|last3=Goda|first3=Sailaja A.|last4=Kasicki|first4=Stefan|last5=Hunt|first5=Mark J.|date=June 2013|title=Antipsychotic compounds differentially modulate high-frequency oscillations in the rat nucleus accumbens: a comparison of first- and second-generation drugs|journal=The International Journal of Neuropsychopharmacology|volume=16|issue=5|pages=1009–1020|doi=10.1017/S1461145712001034|issn=1469-5111|pmid=23171738|doi-access=free}}{{Cite journal|last1=Goda|first1=Sailaja A.|last2=Olszewski|first2=Maciej|last3=Piasecka|first3=Joanna|last4=Rejniak|first4=Karolina|last5=Whittington|first5=Miles A.|last6=Kasicki|first6=Stefan|last7=Hunt|first7=Mark J.|date=August 2015|title=Aberrant high frequency oscillations recorded in the rat nucleus accumbens in the methylazoxymethanol acetate neurodevelopmental model of schizophrenia|url=http://dx.doi.org/10.1016/j.pnpbp.2015.03.016|journal=Progress in Neuro-Psychopharmacology and Biological Psychiatry|volume=61|pages=44–51|doi=10.1016/j.pnpbp.2015.03.016|pmid=25862088|s2cid=13965042|issn=0278-5846}}
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. 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.{{Cite journal|last1=Haufler|first1=Darrell|last2=Pare|first2=Denis|date=2014-07-01|title=High-frequency oscillations are prominent in the extended amygdala|journal=Journal of Neurophysiology|volume=112|issue=1|pages=110–119|doi=10.1152/jn.00107.2014|issn=0022-3077|pmc=4064387|pmid=24717353}}{{Cite journal|last1=Zhong|first1=Weiwei|last2=Ciatipis|first2=Mareva|last3=Wolfenstetter|first3=Thérèse|last4=Jessberger|first4=Jakob|last5=Müller|first5=Carola|last6=Ponsel|first6=Simon|last7=Yanovsky|first7=Yevgenij|last8=Brankačk|first8=Jurij|last9=Tort|first9=Adriano B. L.|last10=Draguhn|first10=Andreas|date=2017-04-25|title=Selective entrainment of gamma subbands by different slow network oscillations|journal=Proceedings of the National Academy of Sciences of the United States of America|volume=114|issue=17|pages=4519–4524|doi=10.1073/pnas.1617249114|issn=0027-8424|pmc=5410835|pmid=28396398|doi-access=free|bibcode=2017PNAS..114.4519Z }} 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).{{Cite journal|last1=Ylinen|first1=A.|last2=Bragin|first2=A.|last3=Nádasdy|first3=Z.|last4=Jandó|first4=G.|last5=Szabó|first5=I.|last6=Sik|first6=A.|last7=Buzsáki|first7=G.|date=January 1995|title=Sharp wave-associated high-frequency oscillation (200 Hz) in the intact hippocampus: network and intracellular mechanisms|journal=The Journal of Neuroscience|volume=15|issue=1 Pt 1|pages=30–46|doi=10.1523/JNEUROSCI.15-01-00030.1995|issn=0270-6474|pmc=6578299|pmid=7823136}} 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.{{Cite journal|last1=Kucewicz|first1=Michal T.|last2=Cimbalnik|first2=Jan|last3=Matsumoto|first3=Joseph Y.|last4=Brinkmann|first4=Benjamin H.|last5=Bower|first5=Mark R.|last6=Vasoli|first6=Vincent|last7=Sulc|first7=Vlastimil|last8=Meyer|first8=Fred|last9=Marsh|first9=W. R.|last10=Stead|first10=S. M.|last11=Worrell|first11=Gregory A.|date=August 2014|title=High frequency oscillations are associated with cognitive processing in human recognition memory|journal=Brain|volume=137|issue=8|pages=2231–2244|doi=10.1093/brain/awu149|issn=0006-8950|pmc=4107742|pmid=24919972}} Another example of physiological HFO of around 300 Hz, was found in subthalamic nucleus,{{Cite journal|last=Foffani|first=G.|date=2003-06-23|title=300-Hz subthalamic oscillations in Parkinson's disease|journal=Brain|language=en|volume=126|issue=10|pages=2153–2163|doi=10.1093/brain/awg229|pmid=12937087|issn=1460-2156|doi-access=free}} 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.{{Cite journal|last1=Burnos|first1=Sergey|last2=Fedele|first2=Tommaso|last3=Schmid|first3=Olivier|last4=Krayenbühl|first4=Niklaus|last5=Sarnthein|first5=Johannes|date=2016-01-01|title=Detectability of the somatosensory evoked high frequency oscillation (HFO) co-recorded by scalp EEG and ECoG under propofol|url= |journal=NeuroImage: Clinical|language=en|volume=10|pages=318–325|doi=10.1016/j.nicl.2015.11.018|pmid=26900572|pmc=4723731|issn=2213-1582}} 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.{{Cite journal|last1=Ozaki|first1=Isamu|last2=Hashimoto|first2=Isao|date=2011-10-01|title=Exploring the physiology and function of high-frequency oscillations (HFOs) from the somatosensory cortex|url=http://www.sciencedirect.com/science/article/pii/S1388245711003750|journal=Clinical Neurophysiology|language=en|volume=122|issue=10|pages=1908–1923|doi=10.1016/j.clinph.2011.05.023|pmid=21724458|s2cid=7628474|issn=1388-2457}} 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.{{Cite journal|last1=Ooba|first1=Hiroshi|last2=Abe|first2=Tatsuya|last3=Kamida|first3=Tohru|last4=Anan|first4=Mitsuhiro|last5=Morishige|first5=Masaki|last6=Fujiki|first6=Minoru|date=April 2010|title=Increasing high-frequency oscillations (HFOs) in patients with brain tumours: implication for increasing amplitude of N20|url=https://pubmed.ncbi.nlm.nih.gov/20097127/|journal=Clinical Neurophysiology|volume=121|issue=4|pages=474–481|doi=10.1016/j.clinph.2009.12.007|issn=1872-8952|pmid=20097127|s2cid=206793052}} 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.{{Cite journal|last1=Murakami|first1=Takenobu|last2=Sakuma|first2=Kenji|last3=Nakashima|first3=Kenji|date=2008-12-01|title=Somatosensory evoked potentials and high-frequency oscillations in athletes|url=http://www.sciencedirect.com/science/article/pii/S138824570800936X|journal=Clinical Neurophysiology|language=en|volume=119|issue=12|pages=2862–2869|doi=10.1016/j.clinph.2008.09.002|pmid=18849191|s2cid=30129908|issn=1388-2457}}
= 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.{{Cite journal|last1=Gobbelé|first1=René|last2=Waberski|first2=Till Dino|last3=Dieckhöfer|first3=Anne|last4=Kawohl|first4=Wolfram|last5=Klostermann|first5=Fabian|last6=Curio|first6=Gabriel|last7=Buchner|first7=Helmut|date=July 2003|title=Patterns of disturbed impulse propagation in multiple sclerosis identified by low and high frequency somatosensory evoked potential components|url=https://pubmed.ncbi.nlm.nih.gov/14530742/|journal=Journal of Clinical Neurophysiology|volume=20|issue=4|pages=283–290|doi=10.1097/00004691-200307000-00008|issn=0736-0258|pmid=14530742|s2cid=24099633}}
- HFO (>80 Hz) occur during epileptic seizure onset.{{Cite journal|last1=Zijlmans|first1=Maeike|last2=Jiruska|first2=Premysl|last3=Zelmann|first3=Rina|last4=Leijten|first4=Frans S. S.|last5=Jefferys|first5=John G. R.|last6=Gotman|first6=Jean|date=February 2012|title=High-frequency oscillations as a new biomarker in epilepsy|journal=Annals of Neurology|volume=71|issue=2|pages=169–178|doi=10.1002/ana.22548|issn=1531-8249|pmc=3754947|pmid=22367988}}{{Cite journal|last1=Frauscher|first1=Birgit|last2=Bartolomei|first2=Fabrice|last3=Kobayashi|first3=Katsuhiro|last4=Cimbalnik|first4=Jan|last5=van't Klooster|first5=Maryse A.|last6=Rampp|first6=Stefan|last7=Otsubo|first7=Hiroshi|last8=Höller|first8=Yvonne|last9=Wu|first9=Joyce Y.|last10=Asano|first10=Eishi|last11=Engel|first11=Jerome|date=August 2017|title=High-frequency oscillations: The state of clinical research|journal=Epilepsia|volume=58|issue=8|pages=1316–1329|doi=10.1111/epi.13829|issn=0013-9580|pmc=5806699|pmid=28666056}}
- Disruption in the HFO (200–500 Hz) synchronization in subthalamic nucleus is related to Parkinson's disease symptoms.{{Cite journal|last1=Yang|first1=Andrew I.|last2=Vanegas|first2=Nora|last3=Lungu|first3=Codrin|last4=Zaghloul|first4=Kareem A.|date=2014-09-17|title=Beta-coupled high-frequency activity and beta-locked neuronal spiking in the subthalamic nucleus of Parkinson's disease|journal=The Journal of Neuroscience|volume=34|issue=38|pages=12816–12827|doi=10.1523/JNEUROSCI.1895-14.2014|issn=1529-2401|pmc=4166162|pmid=25232117}}
- HFOs are visible in different brain regions just after cardiac-arrest and are linked to near-death states.{{Cite journal|last1=Borjigin|first1=Jimo|last2=Lee|first2=UnCheol|last3=Liu|first3=Tiecheng|last4=Pal|first4=Dinesh|last5=Huff|first5=Sean|last6=Klarr|first6=Daniel|last7=Sloboda|first7=Jennifer|last8=Hernandez|first8=Jason|last9=Wang|first9=Michael M.|last10=Mashour|first10=George A.|date=2013-08-27|title=Surge of neurophysiological coherence and connectivity in the dying brain|journal=Proceedings of the National Academy of Sciences of the United States of America|volume=110|issue=35|pages=14432–14437|doi=10.1073/pnas.1308285110|issn=1091-6490|pmc=3761619|pmid=23940340|bibcode=2013PNAS..11014432B|doi-access=free}}
- 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).{{Cite journal|last1=Hunt|first1=Mark J.|last2=Olszewski|first2=Maciej|last3=Piasecka|first3=Joanna|last4=Whittington|first4=Miles A.|last5=Kasicki|first5=Stefan|date=2015|title=Effects of NMDA receptor antagonists and antipsychotics on high frequency oscillations recorded in the nucleus accumbens of freely moving mice|journal=Psychopharmacology|volume=232|issue=24|pages=4525–4535|doi=10.1007/s00213-015-4073-0|issn=0033-3158|pmc=4646921|pmid=26446869}}{{Cite journal|last1=Hunt|first1=Mark J|last2=Kasicki|first2=Stefan|date=2013-07-17|title=A systematic review of the effects of NMDA receptor antagonists on oscillatory activity recorded in vivo|url=http://dx.doi.org/10.1177/0269881113495117|journal=Journal of Psychopharmacology|volume=27|issue=11|pages=972–986|doi=10.1177/0269881113495117|pmid=23863924|s2cid=31344362|issn=0269-8811}}
= NMDA receptor hypofunction HFO =
File:Hfo_rat.gif reconstruction (done with kCSD method,{{Cite journal|last1=Chintaluri|first1=Chaitanya|last2=Bejtka|first2=Marta|last3=Średniawa|first3=Władysław|last4=Czerwiński|first4=Michał|last5=Dzik|first5=Jakub M.|last6=Jędrzejewska-Szmek|first6=Joanna|last7=Kondrakiewicz|first7=Kacper|last8=Kublik|first8=Ewa|last9=Wójcik|first9=Daniel K.|date=2021-05-14|title=What we can and what we cannot see with extracellular multielectrodes|journal=PLOS Computational Biology|language=en|volume=17|issue=5|pages=e1008615|doi=10.1371/journal.pcbi.1008615|pmid=33989280|pmc=8153483|bibcode=2021PLSCB..17E8615C|issn=1553-7358|doi-access=free}} 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,{{Cite journal|last1=Hunt|first1=Mark Jeremy|last2=Raynaud|first2=Beryl|last3=Garcia|first3=Rene|date=2006-12-01|title=Ketamine dose-dependently induces high-frequency oscillations in the nucleus accumbens in freely moving rats|url=https://pubmed.ncbi.nlm.nih.gov/16650831/|journal=Biological Psychiatry|volume=60|issue=11|pages=1206–1214|doi=10.1016/j.biopsych.2006.01.020|issn=0006-3223|pmid=16650831|s2cid=22548264}}{{Cite journal|last1=Frohlich|first1=Joel|last2=Van Horn|first2=John D.|date=April 2014|title=Reviewing the ketamine model for schizophrenia|journal=Journal of Psychopharmacology|volume=28|issue=4|pages=287–302|doi=10.1177/0269881113512909|issn=1461-7285|pmc=4133098|pmid=24257811}}{{Cite journal|last1=Phillips|first1=K.G.|last2=Cotel|first2=M.C.|last3=McCarthy|first3=A.P.|last4=Edgar|first4=D.M.|last5=Tricklebank|first5=M.|last6=O'Neill|first6=M.J.|last7=Jones|first7=M.W.|last8=Wafford|first8=K.A.|date=March 2012|title=Differential effects of NMDA antagonists on high frequency and gamma EEG oscillations in a neurodevelopmental model of schizophrenia|url=https://linkinghub.elsevier.com/retrieve/pii/S0028390811001511|journal=Neuropharmacology|language=en|volume=62|issue=3|pages=1359–1370|doi=10.1016/j.neuropharm.2011.04.006|pmid=21521646|s2cid=23058003}}{{Cite journal|last1=Hansen|first1=Ingeborg H.|last2=Agerskov|first2=Claus|last3=Arvastson|first3=Lars|last4=Bastlund|first4=Jesper F.|last5=Sørensen|first5=Helge B. D.|last6=Herrik|first6=Kjartan F.|date=July 2019|title=Pharmaco-electroencephalographic responses in the rat differ between active and inactive locomotor states|journal=The European Journal of Neuroscience|volume=50|issue=2|pages=1948–1971|doi=10.1111/ejn.14373|issn=1460-9568|pmc=6806018|pmid=30762918}} which is also a pharmacological model of schizophrenia. These NMDA receptor dependent fast oscillations were detected in different brain areas including hippocampus,{{Cite journal|last1=Caixeta|first1=Fábio V.|last2=Cornélio|first2=Alianda M.|last3=Scheffer-Teixeira|first3=Robson|last4=Ribeiro|first4=Sidarta|last5=Tort|first5=Adriano B. L.|date=2013-08-02|title=Ketamine alters oscillatory coupling in the hippocampus|journal=Scientific Reports|volume=3|page=2348|doi=10.1038/srep02348|issn=2045-2322|pmc=3731648|pmid=23907109|bibcode=2013NatSR...3.2348C}} nucleus accumbens and prefrontal cortex regions.{{Cite journal|last1=Pittman-Polletta|first1=Benjamin|last2=Hu|first2=Kun|last3=Kocsis|first3=Bernat|date=2018-08-02|title=Subunit-specific NMDAR antagonism dissociates schizophrenia subtype-relevant oscillopathies associated with frontal hypofunction and hippocampal hyperfunction|journal=Scientific Reports|volume=8|issue=1|page=11588|doi=10.1038/s41598-018-29331-8|issn=2045-2322|pmc=6072790|pmid=30072757|bibcode=2018NatSR...811588P}} 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. 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.{{Cite journal|last1=Hunt|first1=Mark Jeremy|last2=Adams|first2=Natalie E.|last3=Średniawa|first3=Władysław|last4=Wójcik|first4=Daniel K.|last5=Simon|first5=Anna|last6=Kasicki|first6=Stefan|last7=Whittington|first7=Miles Adrian|date=January 2019|title=The olfactory bulb is a source of high-frequency oscillations (130–180 Hz) associated with a subanesthetic dose of ketamine in rodents|journal=Neuropsychopharmacology|language=en|volume=44|issue=2|pages=435–442|doi=10.1038/s41386-018-0173-y|pmid=30140046|pmc=6300534|issn=1740-634X|doi-access=free}}{{Cite journal|last1=Wróbel|first1=Jacek|last2=Średniawa|first2=Władysław|last3=Jurkiewicz|first3=Gabriela|last4=Żygierewicz|first4=Jarosław|last5=Wójcik|first5=Daniel K.|last6=Whittington|first6=Miles Adrian|last7=Hunt|first7=Mark Jeremy|date=2020-11-04|title=Nasal respiration is necessary for ketamine-dependent high frequency network oscillations and behavioral hyperactivity in rats|journal=Scientific Reports|language=en|volume=10|issue=1|pages=18981|doi=10.1038/s41598-020-75641-1|pmid=33149202|pmc=7642442|bibcode=2020NatSR..1018981W|issn=2045-2322|doi-access=free}} HFO in the bulb is generated by local excitatory-inhibitory circuits modulated by breathing rhythm and may be also recorded under ketamine-xylazine anesthesia.{{Cite journal|last1=Średniawa|first1=Władysław|last2=Wróbel|first2=Jacek|last3=Kublik|first3=Ewa|last4=Wójcik|first4=Daniel Krzysztof|last5=Whittington|first5=Miles Adrian|last6=Hunt|first6=Mark Jeremy|date=2021-03-18|title=Network and synaptic mechanisms underlying high frequency oscillations in the rat and cat olfactory bulb under ketamine-xylazine anesthesia|journal=Scientific Reports|language=en|volume=11|issue=1|pages=6390|doi=10.1038/s41598-021-85705-5|pmid=33737621|pmc=7973548|issn=2045-2322|doi-access=free}} This findings may aid understanding early symptoms of schizophrenia patients and their relatives, that can suffer from olfactory system impairments.{{Cite journal|last1=Turetsky|first1=Bruce I|last2=Hahn|first2=Chang-Gyu|last3=Arnold|first3=Steven E|last4=Moberg|first4=Paul J|date=February 2009|title=Olfactory Receptor Neuron Dysfunction in Schizophrenia|journal=Neuropsychopharmacology |volume=34|issue=3|pages=767–774|doi=10.1038/npp.2008.139|issn=0893-133X|pmc=3524971|pmid=18754006}}
See also
= Brain waves =
- Delta wave – (0.1 – 3 Hz)
- Theta wave – (4 – 7 Hz)
- Mu wave – (7.5 – 12.5 Hz)
- SMR wave – (12.5 – 15.5 Hz)
- Alpha wave – (7 (or 8) – 12 Hz)
- Beta wave – (12 – 30 Hz)
- Gamma wave – (32 – 100 Hz)