Multimodality localization of the sensorimotor cortex in pediatric patients undergoing epilepsy surgery

Clinical article

Carter D. WrayDepartments of Neurology,
Divisions of Pediatric Neurology,

Search for other papers by Carter D. Wray in
jns
Google Scholar
PubMed
Close
 M.D.
,
Tim M. BlakelyBioengineering, and

Search for other papers by Tim M. Blakely in
jns
Google Scholar
PubMed
Close
 M.S.
,
Sandra L. PoliachikDivisions of Pediatric Neurology,
Pediatric Radiology, and

Search for other papers by Sandra L. Poliachik in
jns
Google Scholar
PubMed
Close
 Ph.D.
,
Andrew PoliakovPediatric Radiology, and
Pediatric Neurosurgery, Seattle Children's Hospital; and

Search for other papers by Andrew Poliakov in
jns
Google Scholar
PubMed
Close
 Ph.D.
,
Sharon S. McDanielDepartments of Neurology,
Divisions of Pediatric Neurology,

Search for other papers by Sharon S. McDaniel in
jns
Google Scholar
PubMed
Close
 M.D.
,
Edward J. NovotnyDepartments of Neurology,
Divisions of Pediatric Neurology,
Pediatric Radiology, and
Center for Integrative Brain Research, Seattle Children's Research Institute, and Integrative Brain Imaging Center, University of Washington, Seattle, Washington

Search for other papers by Edward J. Novotny in
jns
Google Scholar
PubMed
Close
 M.D.
,
Kai J. MillerNeurosurgery, University of Washington;

Search for other papers by Kai J. Miller in
jns
Google Scholar
PubMed
Close
 M.D., Ph.D.
, and
Jeffrey G. OjemannNeurosurgery, University of Washington;
Pediatric Radiology, and
Pediatric Neurosurgery, Seattle Children's Hospital; and
Center for Integrative Brain Research, Seattle Children's Research Institute, and Integrative Brain Imaging Center, University of Washington, Seattle, Washington

Search for other papers by Jeffrey G. Ojemann in
jns
Google Scholar
PubMed
Close
 M.D.
View More View Less
Restricted access

Purchase Now

USD  $45.00

JNS + Pediatrics - 1 year subscription bundle (Individuals Only)

USD  $525.00

JNS + Pediatrics + Spine - 1 year subscription bundle (Individuals Only)

USD  $624.00
USD  $45.00
USD  $525.00
USD  $624.00
Print or Print + Online Sign in

Object

The gold-standard method for determining cortical functional organization in the context of neurosurgical intervention is electrical cortical stimulation (ECS), which disrupts normal cortical function to evoke movement. This technique is imprecise, however, as motor responses are not limited to the precentral gyrus. Electrical cortical stimulation also can trigger seizures, is not always tolerated, and is often unsuccessful, especially in children. Alternatively, endogenous motor and sensory signals can be mapped by somatosensory evoked potentials (SSEPs), functional MRI (fMRI), and electrocorticography of high gamma (70–150 Hz) signal power, which reflect normal cortical function. The authors evaluated whether these 4 modalities of mapping sensorimotor function in children produce concurrent results.

Methods

The authors retrospectively examined the charts of all patients who underwent epilepsy surgery at Seattle Children's Hospital between July 20, 1999, and July 1, 2011, and they included all patients in whom the primary motor or somatosensory cortex was localized via 2 or more of the following tests: ECS, SSEP, fMRI, or high gamma electrocorticography (hgECoG).

Results

Inclusion criteria were met by 50 patients, whose mean age at operation was 10.6 years. The youngest patient who underwent hgECoG mapping was 2 years and 10 months old, which is younger than any patient reported on in the literature. The authors localized the putative sensorimotor cortex most often with hgECoG, followed by SSEP and fMRI; ECS was most likely to fail to localize the sensorimotor cortex.

Conclusions

Electrical cortical stimulation, SSEP, fMRI, and hgECoG generally produced concordant localization of motor and sensory function in children. When attempting to localize the sensorimotor cortex in children, hgECoG was more likely to produce results, was faster, safer, and did not require cooperation. The hgECoG maps in pediatric patients are similar to those in adult patients published in the literature. The sensorimotor cortex can be mapped by hgECoG and fMRI in children younger than 3 years old to localize cortical function.

Abbreviations used in this paper:

BOLD = blood oxygen level–dependent; ECS = electrical cortical stimulation; fMRI = functional MRI; hgECoG = high gamma electrocorticography; SSEP = somatosensory evoked potential.
  • Collapse
  • Expand
  • 1

    Acharya S, , Fifer MS, , Benz HL, , Crone NE, & Thakor NV: Electrocorticographic amplitude predicts finger positions during slow grasping motions of the hand. J Neural Eng 7:046002, 2010

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 2

    Brovelli A, , Lachaux JP, , Kahane P, & Boussaoud D: High gamma frequency oscillatory activity dissociates attention from intention in the human premotor cortex. Neuroimage 28:154164, 2005

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 3

    Brunner P, , Ritaccio AL, , Lynch TM, , Emrich JF, , Wilson JA, & Williams JC, et al.: A practical procedure for real-time functional mapping of eloquent cortex using electrocorticographic signals in humans. Epilepsy Behav 15:278286, 2009

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 4

    Crone NE, , Miglioretti DL, , Gordon B, & Lesser RP: Functional mapping of human sensorimotor cortex with electrocorticographic spectral analysis. No II: Event-related synchronization in the gamma band. Brain 121:23012315, 1998

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 5

    Crone NE, , Sinai A, & Korzeniewska A: High-frequency gamma oscillations and human brain mapping with electrocorticography. Prog Brain Res 159:275295, 2006

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 6

    Fandino J, , Kollias SS, , Wieser HG, , Valavanis A, & Yonekawa Y: Intraoperative validation of functional magnetic resonance imaging and cortical reorganization patterns in patients with brain tumors involving the primary motor cortex. J Neurosurg 91:238250, 1999

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 7

    Haglund MM, , Berger MS, , Shamseldin M, , Lettich E, & Ojemann GA: Cortical localization of temporal lobe language sites in patients with gliomas. Neurosurgery 34:567576, 1994

    • Search Google Scholar
    • Export Citation
  • 8

    Hermes D, , Miller KJ, , Vansteensel MJ, , Aarnoutse EJ, , Leijten FS, & Ramsey NF: Neurophysiologic correlates of fMRI in human motor cortex. Hum Brain Mapp [epub ahead of print], 2011

    • Search Google Scholar
    • Export Citation
  • 9

    Ikeda A, & Shibasaki H, Cortical mapping using evoked potentials and Bereitschaftspotentials. Luders H: Textbook of Epilepsy Surgery London, Informa Healthcare, 2008. 10361048

    • Search Google Scholar
    • Export Citation
  • 10

    Keles GE, , Lundin DA, , Lamborn KR, , Chang EF, , Ojemann G, & Berger MS: Intraoperative subcortical stimulation mapping for hemispherical perirolandic gliomas located within or adjacent to the descending motor pathways: evaluation of morbidity and assessment of functional outcome in 294 patients. J Neurosurg 100:369375, 2004

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 11

    Khursheed F, , Tandon N, , Tertel K, , Pieters TA, , Disano MA, & Ellmore TM: Frequency-specific electrocorticographic correlates of working memory delay period fMRI activity. Neuroimage 56:17731782, 2011

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 12

    Lachaux JP, , Fonlupt P, , Kahane P, , Minotti L, , Hoffmann D, & Bertrand O, et al.: Relationship between task-related gamma oscillations and BOLD signal: new insights from combined fMRI and intracranial EEG. Hum Brain Mapp 28:13681375, 2007

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13

    Legatt AD, & Kader A: Topography of the initial cortical component of the median nerve somatosensory evoked potential. Relationship to central sulcus anatomy. J Clin Neurophysiol 17:321325, 2000

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 14

    Leuthardt EC, , Miller K, , Anderson NR, , Schalk G, , Dowling J, & Miller J, et al.: Electrocorticographic frequency alteration mapping: a clinical technique for mapping the motor cortex. Neurosurgery 60:4 Suppl 2 260271, 2007

    • Search Google Scholar
    • Export Citation
  • 15

    Martino J, , Gabarrós A, , Deus J, , Juncadella M, , Acebes JJ, & Torres A, et al.: Intrasurgical mapping of complex motor function in the superior frontal gyrus. Neuroscience 179:131142, 2011

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 16

    Miller KJ, , Abel TJ, , Hebb AO, & Ojemann JG: Rapid online language mapping with electrocorticography. Clinical article. J Neurosurg Pediatr 7:482490, 2011

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 17

    Miller KJ, , denNijs M, , Shenoy P, , Miller JW, , Rao RP, & Ojemann JG: Real-time functional brain mapping using electrocorticography. Neuroimage 37:504507, 2007

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 18

    Miller KJ, , Leuthardt EC, , Schalk G, , Rao RP, , Anderson NR, & Moran DW, et al.: Spectral changes in cortical surface potentials during motor movement. J Neurosci 27:24242432, 2007

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 19

    Miller KJ, , Makeig S, , Hebb AO, , Rao RPN, , den Nijs M, & Ojemann JG: Cortical electrode localization from X-rays and simple mapping for electrocorticographic research: the “Location on Cortex” (LOC) package for MATLAB. J Neurosci Methods 162:303308, 2007

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 20

    Miller KJ, , Schalk G, , Fetz EE, , den Nijs M, , Ojemann JG, & Rao RPN: Cortical activity during motor execution, motor imagery, and imagery-based online feedback. Proc Natl Acad Sci U S A 107:44304435, 2010

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 21

    Miller KJ, , Zanos S, , Fetz EE, , den Nijs M, & Ojemann JG: Decoupling the cortical power spectrum reveals real-time representation of individual finger movements in humans. J Neurosci 29:31323137, 2009

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 22

    Mukamel R, , Gelbard H, , Arieli A, , Hasson U, , Fried I, & Malach R: Coupling between neuronal firing, field potentials, and FMRI in human auditory cortex. Science 309:951954, 2005

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 23

    Pfurtscheller G, , Graimann B, , Huggins JE, , Levine SP, & Schuh LA: Spatiotemporal patterns of beta desynchronization and gamma synchronization in corticographic data during self-paced movement. Clin Neurophysiol 114:12261236, 2003

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 24

    Pfurtscheller G, & Lopes da Silva FH: Event-related EEG/MEG synchronization and desynchronization: basic principles. Clin Neurophysiol 110:18421857, 1999

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 25

    Reis J, & Rosenow F, Eloquent cortex and tract: overview and noninvasive evaluation methods. Luders H: Textbook of Epilepsy Surgery London, Informa Healthcare, 2008. 869880

    • Search Google Scholar
    • Export Citation
  • 26

    Schalk G, , McFarland DJ, , Hinterberger T, , Birbaumer N, & Wolpaw JR: BCI2000: a general-purpose brain-computer interface (BCI) system. IEEE Trans Biomed Eng 51:10341043, 2004

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 27

    Schule S, , McIntyre C, & Luders H, General principles of cortical mapping by electrical stimulation. Luders H: Text-book of Epilepsy Surgery London, Informa Healthcare, 2008. 961977

    • Search Google Scholar
    • Export Citation
  • 28

    Shurtleff H, , Warner M, , Poliakov A, , Bournival B, , Shaw DW, & Ishak G, et al.: Functional magnetic resonance imaging for presurgical evaluation of very young pediatric patients with epilepsy. Clinical article. J Neurosurg Pediatr 5:500506, 2010

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 29

    Vapnik VN: The Nature of Statistical Learning Theory New York, Springer, 2000

Metrics

All Time Past Year Past 30 Days
Abstract Views 1796 660 36
Full Text Views 100 5 1
PDF Downloads 134 5 2
EPUB Downloads 0 0 0