High Frequency Oscillation in
scalp EEG and its utilization
Hisanori Hasegawa, M.D.
History
• The customarily recorded EEG frequency range
has been 0.3-70Hz
• Jasper and Andrews recorded 35-45/sec activity
superinposed on the posterior alpha (1938)
• The study of gamma frequency EEG had been rare
until 1980’s.
• Investigation of Gray (1988) focused on 40-60/sec
activity in visual cortex of cats.
• Human EEG activity >80Hz were rarely studied
before.
High frequency oscillation
• HFO: 80-200Hz
• Fast Ripple: 200-600Hz
• Ripples recoded in
– Rodents Buzsaki 1982, Ylinen 1995
– Primate Skaggs 2007
– Human Bragin 1999, Staba 2004
Niedermeyer (2001)
• “Ripples were practically absent in the neocortex
but common in the depth leads, especially
hippocampus.”
• “Neocortical spiking often assumed a rhythmic
character (6-7Hz). Ripples and spikes occurred
either independently or at times, with a fixed time
lag”
• “The role of ultrafast frequencies in
neruocognitive function is in need of further
elusidation”
Engel (2009)
Epilepsia 50,598-604, 2009 (commentary)
• High Frequency Oscillation 80-200Hz
• Frequent Ripple 250-600Hz
Worrell
Brain 2004, 127, 1496-1506
• “HFO and seizure generation in neocortical
epilepsy”
– Neocortical HFO 60-100Hz localize in seizure
in intracranial electrodes (6/23)
– The majority of seizure (62%) showed increase
of HFO 20 min prior to the seizure onset.
Urrestarazu
Epilepsia 47(9)1465-76:2006
• HF Intracerabral EEG activity (100-500Hz)
– Recorded in intracranial electrodes
• 100-250 Hz ripples
–
–
–
–
–
80-160 Hz ripples are epileptogenic
250-500 Hz were reported as FR
FR is more lateralized to ipsilateral HP
FR may relate to seizure onset
Recorded LFF 500 Hz, sampling frequency 2000 Hz
Bagshaw
Epilepsia 50(4)617-628, 2009
• Recorded in intracranial macroelectrodes
• HFO >80Hz in preictal period were more
prominent in the SOZ
• Findings were more reliable if exclude
awake state and REM sleep state.
Jacobs
Epilepsia 1-13, 2009
• HF 80-500Hz in periictal period
• HFO are seen in non-REM sleep. Accurate
sleep staging is not necessary otherwise.
• Jacobs Epilepsia 49(11), 1893-1907, 2008
• Interictal HF are indicator of seizure onset
area
• HFO are largely independent of spikes
• Most frequent in mesial temporal structure
Staba
Epilepsia 48(11)2130-2138, 2007
• Increased FR to Ripple rations correlate
with reduced hippocampal volume.
• Derangement of excitatory and inhibitory
circuitry in CA1 that increase reccurent
excitation or neuronal synchronization or
both may increase FR and decrease in
Ripple
Lutz
PNAS, Nov 16, 2004
• 8 Buddist monks, 10 healthy controls
• 128 ch scalp EEG recordings, Sf=500 Hz,
LFF=0.1, HFF=200.
• Robust γ-band oscillation and long distuce
phase synchrony in meditated state by scalp
EEG.
Scalp HF recording
•
•
•
Focal ictal βdischarge in scalp EEG
Gregory Worrell
Epilepsia 43(3)277-282, 2002
•
•
•
Paroxysmal Fast Activity in InterictalScalp EEG
Joyce Wu
Epilepsy Research 82,99-106, 2008
•
•
•
Trancient Induced gamma-band Response in EEG
K Kobayashi
Neuron 58,429-441, May 8, 2008
•
•
•
Very fast ryhthmic activity in scalp EEG
K Kobayashi
Epilepsia 45(5)488-496, 2006
•
•
•
Reevaluating the mechanisms of focal ictogenesis: The role of low-voltage fast
Marco de Cartis
Epilepsia 50(12)2514-2525, 2009
HFO recording on scalp surface
• So far, most of the HF research papers were
written using intracranial depth electrode
recordings
• Scalp recording has difficulties.
Difficulties in scalp HF
recordings
• Susceptible to artifacts
–
–
–
–
–
–
Nonspecific movement
Muscle artifacts
Eating
Swallowing
Sneezing
Vocalization
• Attenuated by skull bone, skin, fat, dura,
CSF by conduction resistance.
Otsubo
“HFO of ictal muscle activity and epileptiform discharges”
J Clin Neurophysiology, 119(2008), 862-868
• Described feature of EMG artifacts which
mimics EEG-HF
– Muscle HF artifacts are random scattered HFO
without specific frequency band.
• Epileptogenic HF had sustained frequency band
– Muscle HF artifact may stay in one place
without evolution
Evaluation of Scalp recording HF
• Sampling frequency 1000Hz so that scalp EEG
may record up to 300Hz reliably.
• Manual selection of sustained frequency behavior
• Visually observed movement should be excluded.
• Search during sleep state. Searching HF is
extremely difficult during awake state due to
varieties of artifacts.
Example
Extend to 5 seconds window
Evidence of Development
Working Hypothesis in Scalp
Permeating HF (SPHF) recording
1. SPHF is reasonably recorded up to 150 Hz
2. SPHF is reasonably identifiable in sleep
state
3. SPHF is recordable with appropriate
sampling frequency. (How high can you
go?)
4. SPHF may still correlate with seizure onset
zone if recorded with seizure.
Pilot study findings
Confirmatory Study
• Routine out-patient EEG recorded 2001-2007 using
2000Hz sampling frequency. The EEG were not recorded
for the purpose of HF analysis.
• This is ad hoc review of abnormal EEG recordings out of
the data.
• 286 abnormal EEGs for various reasons (back ground
slowing, focal slowing, IID, electrographic seizures, etc)
were identified.
• These 286 EEGs were reviewed to search for reliable
findings of SPHF.
Swallowing
Snoring

Eye Movements
Muscle Artifacts
Teeth grinding

Harmonics
Examples of SPHF
Results 1
• Among the 286 EEGs, 107 were awake
state recordings, and 177 were awakeasleep state, and 2 were moderately sever
encephalopathy findings.
Awake
Awake+sleep
Encephalopathic
HF +
171
45
1
HF -
6
62
1
Result 2
• Among the 286 abnormal EEGs, 65 had epileptiform
discharges.
• 38 showed HF ipsilateral to localization of interictal
epileptiform discharges.
• 18 showed HF contralateral to localization of interictal
epileptiform discharges.
• 9 had bilateral HF distribution.
• 3 had HF without interictal epileptiform discharges.
Results 3
• If HF was seen in the ipsilateral hemisphere
to the localization of primary IID focus, the
HF frequency tend to be faster than
contralateral localization.
Frequency range 35-50 Hz
50-65 Hz
>65 Hz
Ipsilateral
9
11
18
Contralateral
6
6
6
Conclusions
• Given that routine EEG recording was abnormal, these
EEGs were recorded with Sampling frequency 2000 Hz.
• Detection of the HF is not our routine EEG analysis
because of many technical challenges to exclude artifacts
of various source. Nevertheless, careful re-reading of EEG
revealed scalp permeating HF. In this ad hoc review study,
realistically identifiable HF was no faster than 150 Hz.
Therefore, 450-500 Hz SF may be sufficient for this kind
of review study in future.