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Continuous EEG-correlated fMRI in epilepsy
International Congress Series 1232 (2002) 719 – 721
Continuous EEG-correlated f MRI in epilepsy Afraim Salek-Haddadi a,b,*, Louis Lemieux a,b, Martin Merschhemke a,b, Philip J. Allen c, David R. Fish c a
Epilepsy Research Group, Institute of Neurology, University College London, Queen Square, London, UK b MRI Unit, National Society for Epilepsy, Chalfont St. Peter, Buckinghamshire, SL9 0RJ, UK c Department of Clinical Neurophysiology, National Hospital for Neurology and Neurosurgery, Queen Square, London, UK
Keywords: EEG; Event-related fMRI; Spikes; Epilepsy
1. Introduction Limited EEG monitoring within the MR scanner is possible [1] and has been applied to study a diverse range of EEG phenomena [2]. It is, however, limited by three major issues: patient safety, image quality and EEG quality. Current-limiting resistors and the fibre optic isolation of subjects within the scanner now provide good safety [3]. Likewise, the careful selection of conductors and RFshielded equipment help minimise interference to the images [4] so, the remaining set of issues centre on EEG quality. Pulse artefact (often referred to as ‘cardioballistogram’) arises from the currents induced through blood or pulsating body movement related to the cardiac cycle [2]. These are variable and may be several times the scalp voltages with very sharp morphology making EEG interpretation impossible, particularly at higher field strengths. The short-term consistency and time-locked nature of this phenomenon, however, has allowed for the removal [5] and the above developments together have permitted the recording of good quality EEG inside the scanner [6]. Still, the rapid gradient changes necessitated by ultra fast imaging sequences induce voltages within the EEG several hundred times greater than those recorded from the scalp. The EEG is, therefore, masked completely by the imaging artefact during the image
* Corresponding author. MRI Unit, National Society for Epilepsy, Chalfont St. Peter, Buckinghamshire SL9 0RJ, UK. Tel.: +44-1494-874646; fax: +44-1494-875666. E-mail address: [email protected] (A. Salek-Haddadi).
0531-5131/02 D 2002 Elsevier Science B.V. All rights reserved. PII: S 0 5 3 1 - 5 1 3 1 ( 0 1 ) 0 0 8 0 7 - X
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A. Salek-Haddadi et al. / International Congress Series 1232 (2002) 719–721
acquisition itself, remaining interpretable only in between [2]. For the first time now, we have been using a technique for removing imaging artefact [7] to allow for uninterrupted good quality EEG recording throughout fMRI acquisition in the study of epilepsy [8].
2. Methods Ethical approval was obtained from the local ethical committee of the National Hospital for Neurology and Neurosurgery along with written consent from the patient. Data were obtained from nine patients with frequent focal interictal epileptiform discharges. Imaging was performed on a GE Horizon Echospeed 1.5 Tesla Scanner using a continuous BOLD-fMRI sequence (TE/TR 40/3000, 215 mm Interleaved Slices, FOV=2424 cm, 6464 Matrix). Seven hundred volumes were acquired over a 35min interval. Twelve channels of EEG (Fp1/Fp2, F7/F8, T3/T4, T5/T6, O1/O2, Cz and Pz) were recorded simultaneously with an in-house MR-compatible recording system using gold electrodes fitted with 10 kV current-limiting resistors [3]. Following pulse and image artefact removal (online and offline), epileptiform discharges were classified and time coded. SPM99 [http:www.fil.ion.ucl.ac.uk/spm/spm99.html] was used to process the fMRI data. Images were realigned and smoothed with a Gaussian kernel of 8 mm full-width half maximum. An event-related design matrix was specified in terms of the onsets of the EEG discharges in units of scans. Statistical parametric maps were constructed within the context of the general linear model and inferences were made after the correction for multiple comparisons.
3. Results Good quality EEG was recorded in all cases allowing for the identification of interictal discharges. Variable degrees of patient motion were evident within the group. Spikerelated BOLD activations were elicited in seven patients with physiologically plausible event-related responses and localisation was broadly consistent with scalp EEG and clinical findings.
4. Conclusions EEG-correlated functional imaging is an exciting field where much progress continues to be made both in the development of techniques and their applications. Patient safety, image quality and EEG quality in terms of pulse and imaging artefacts have each driven technical advances to the point where simultaneous and continuous EEG recording throughout fMRI has become possible, superseding EEG-triggered fMRI. Good quality EEG can be recorded continuously allowing for the identification of epileptiform events with certainty. The localization and continuous study of BOLD (Blood Oxygen Level Dependent) changes in relation to spontaneous EEG events, such as IEDs,
A. Salek-Haddadi et al. / International Congress Series 1232 (2002) 719–721
721
is possible with unparalleled spatiotemporal resolution through event-related fMRI. This non-invasive means of probing the generators of EEG events, bears much promise as a tool in both the scientific and clinical investigations of epilepsy but is at present not without other theoretical, technical and methodological limitations.
References [1] J.R. Ives, S. Warach, F. Schmitt, R.R. Edelman, D.L. Schomer, Monitoring the patient’s EEG during echo planar MRI, Electroencephalogr. Clin. Neurophysiol. 87 (1993) 417 – 420. [2] D.L. Schomer, G. Bonmassar, F. Lazeyras, M. Seeck, A. Blum, K. Anami, et al., EEG-linked functional magnetic resonance imaging in epilepsy and cognitive neurophysiology, J. Clin. Neurophysiol. 17 (2000) 43 – 58. [3] L. Lemieux, P.J. Allen, F. Franconi, M.R. Symms, D.R. Fish, Recording of EEG during fMRI experiments: patient safety, Magn. Reson. Med. 38 (1997) 943 – 952. [4] K. Krakow, P.J. Allen, M.R. Symms, L. Lemieux, O. Josephs, D.R. Fish, EEG recording during fMRI experiments: image quality, Hum. Brain Mapp. 10 (2000) 10 – 15. [5] P.J. Allen, G. Polizzi, K. Krakow, D.R. Fish, L. Lemieux, Identification of EEG events in the MR scanner: the problem of pulse artifact and a method for its subtraction, Neuroimage 8 (1998) 229 – 239. [6] K. Krakow, F.G. Woermann, M.R. Symms, P.J. Allen, L. Lemieux, G.J. Barker, et al., EEG-triggered functional MRI of interictal epileptiform activity in patients with partial seizures, Brain 122 (1999) 1679 – 1688. [7] P.J. Allen, O. Josephs, R. Turner, A method for removing imaging artifact from continuous EEG recorded during functional MRI, Neuroimage 12 (2000) 230 – 239. [8] L. Lemieux, A. Salek-Haddadi, O. Josephs, P. Allen, N. Toms, C. Scott, K. Krakow, R. Turner, D.R. Fish, Event-related fMRI with simultaneous and continuous EEG: description of the method and initial case report, Neuroimage 14 (2001) 780 – 787.
Continuous EEG-correlated f MRI in epilepsy Afraim Salek-Haddadi a,b,*, Louis Lemieux a,b, Martin Merschhemke a,b, Philip J. Allen c, David R. Fish c a
Epilepsy Research Group, Institute of Neurology, University College London, Queen Square, London, UK b MRI Unit, National Society for Epilepsy, Chalfont St. Peter, Buckinghamshire, SL9 0RJ, UK c Department of Clinical Neurophysiology, National Hospital for Neurology and Neurosurgery, Queen Square, London, UK
Keywords: EEG; Event-related fMRI; Spikes; Epilepsy
1. Introduction Limited EEG monitoring within the MR scanner is possible [1] and has been applied to study a diverse range of EEG phenomena [2]. It is, however, limited by three major issues: patient safety, image quality and EEG quality. Current-limiting resistors and the fibre optic isolation of subjects within the scanner now provide good safety [3]. Likewise, the careful selection of conductors and RFshielded equipment help minimise interference to the images [4] so, the remaining set of issues centre on EEG quality. Pulse artefact (often referred to as ‘cardioballistogram’) arises from the currents induced through blood or pulsating body movement related to the cardiac cycle [2]. These are variable and may be several times the scalp voltages with very sharp morphology making EEG interpretation impossible, particularly at higher field strengths. The short-term consistency and time-locked nature of this phenomenon, however, has allowed for the removal [5] and the above developments together have permitted the recording of good quality EEG inside the scanner [6]. Still, the rapid gradient changes necessitated by ultra fast imaging sequences induce voltages within the EEG several hundred times greater than those recorded from the scalp. The EEG is, therefore, masked completely by the imaging artefact during the image
* Corresponding author. MRI Unit, National Society for Epilepsy, Chalfont St. Peter, Buckinghamshire SL9 0RJ, UK. Tel.: +44-1494-874646; fax: +44-1494-875666. E-mail address: [email protected] (A. Salek-Haddadi).
0531-5131/02 D 2002 Elsevier Science B.V. All rights reserved. PII: S 0 5 3 1 - 5 1 3 1 ( 0 1 ) 0 0 8 0 7 - X
720
A. Salek-Haddadi et al. / International Congress Series 1232 (2002) 719–721
acquisition itself, remaining interpretable only in between [2]. For the first time now, we have been using a technique for removing imaging artefact [7] to allow for uninterrupted good quality EEG recording throughout fMRI acquisition in the study of epilepsy [8].
2. Methods Ethical approval was obtained from the local ethical committee of the National Hospital for Neurology and Neurosurgery along with written consent from the patient. Data were obtained from nine patients with frequent focal interictal epileptiform discharges. Imaging was performed on a GE Horizon Echospeed 1.5 Tesla Scanner using a continuous BOLD-fMRI sequence (TE/TR 40/3000, 215 mm Interleaved Slices, FOV=2424 cm, 6464 Matrix). Seven hundred volumes were acquired over a 35min interval. Twelve channels of EEG (Fp1/Fp2, F7/F8, T3/T4, T5/T6, O1/O2, Cz and Pz) were recorded simultaneously with an in-house MR-compatible recording system using gold electrodes fitted with 10 kV current-limiting resistors [3]. Following pulse and image artefact removal (online and offline), epileptiform discharges were classified and time coded. SPM99 [http:www.fil.ion.ucl.ac.uk/spm/spm99.html] was used to process the fMRI data. Images were realigned and smoothed with a Gaussian kernel of 8 mm full-width half maximum. An event-related design matrix was specified in terms of the onsets of the EEG discharges in units of scans. Statistical parametric maps were constructed within the context of the general linear model and inferences were made after the correction for multiple comparisons.
3. Results Good quality EEG was recorded in all cases allowing for the identification of interictal discharges. Variable degrees of patient motion were evident within the group. Spikerelated BOLD activations were elicited in seven patients with physiologically plausible event-related responses and localisation was broadly consistent with scalp EEG and clinical findings.
4. Conclusions EEG-correlated functional imaging is an exciting field where much progress continues to be made both in the development of techniques and their applications. Patient safety, image quality and EEG quality in terms of pulse and imaging artefacts have each driven technical advances to the point where simultaneous and continuous EEG recording throughout fMRI has become possible, superseding EEG-triggered fMRI. Good quality EEG can be recorded continuously allowing for the identification of epileptiform events with certainty. The localization and continuous study of BOLD (Blood Oxygen Level Dependent) changes in relation to spontaneous EEG events, such as IEDs,
A. Salek-Haddadi et al. / International Congress Series 1232 (2002) 719–721
721
is possible with unparalleled spatiotemporal resolution through event-related fMRI. This non-invasive means of probing the generators of EEG events, bears much promise as a tool in both the scientific and clinical investigations of epilepsy but is at present not without other theoretical, technical and methodological limitations.
References [1] J.R. Ives, S. Warach, F. Schmitt, R.R. Edelman, D.L. Schomer, Monitoring the patient’s EEG during echo planar MRI, Electroencephalogr. Clin. Neurophysiol. 87 (1993) 417 – 420. [2] D.L. Schomer, G. Bonmassar, F. Lazeyras, M. Seeck, A. Blum, K. Anami, et al., EEG-linked functional magnetic resonance imaging in epilepsy and cognitive neurophysiology, J. Clin. Neurophysiol. 17 (2000) 43 – 58. [3] L. Lemieux, P.J. Allen, F. Franconi, M.R. Symms, D.R. Fish, Recording of EEG during fMRI experiments: patient safety, Magn. Reson. Med. 38 (1997) 943 – 952. [4] K. Krakow, P.J. Allen, M.R. Symms, L. Lemieux, O. Josephs, D.R. Fish, EEG recording during fMRI experiments: image quality, Hum. Brain Mapp. 10 (2000) 10 – 15. [5] P.J. Allen, G. Polizzi, K. Krakow, D.R. Fish, L. Lemieux, Identification of EEG events in the MR scanner: the problem of pulse artifact and a method for its subtraction, Neuroimage 8 (1998) 229 – 239. [6] K. Krakow, F.G. Woermann, M.R. Symms, P.J. Allen, L. Lemieux, G.J. Barker, et al., EEG-triggered functional MRI of interictal epileptiform activity in patients with partial seizures, Brain 122 (1999) 1679 – 1688. [7] P.J. Allen, O. Josephs, R. Turner, A method for removing imaging artifact from continuous EEG recorded during functional MRI, Neuroimage 12 (2000) 230 – 239. [8] L. Lemieux, A. Salek-Haddadi, O. Josephs, P. Allen, N. Toms, C. Scott, K. Krakow, R. Turner, D.R. Fish, Event-related fMRI with simultaneous and continuous EEG: description of the method and initial case report, Neuroimage 14 (2001) 780 – 787.