Accessible Unlicensed Requires Authentication Published by De Gruyter February 18, 2013

Assessment of visual function during brain surgery near the visual cortex by intraoperative optical imaging

Stephan B. Sobottka, Tobias Meyer, Matthias Kirsch, Gilfe Reiss, Edmund Koch, Ute Morgenstern and Gabriele Schackert

Abstract

Several functional brain imaging and mapping techniques have been used for the intraoperative identification and preservation of the sensory, motor, and speech areas of the brain. However, intraoperative monitoring and mapping of the visual function is less frequently performed in the clinical routine. To our knowledge, here we demonstrate for the first time that the individual visual cortex can be mapped to the brain surface using a contact-free optical camera system during brain surgery. Intraoperative optical imaging (IOI) was performed by visual stimulation of both eyes using stobe-light flashes. Images were acquired by a camera mounted to a standard surgical microscope. Activity maps could reproducibly be computed by detecting the blood volume-dependent signal changes of the exposed cortex. To the preliminary experience, the new technique seems to be suitable for mapping the visual function in any neurosurgical intervention that requires exposure of the visual cortex. However, the clinical relevance and reliability of the technique need to be confirmed in further studies.


Corresponding author: PD Dr. med. habil. Stephan B. Sobottka, Department of Neurosurgery, University Hospital Carl Gustav Carus, Dresden University of Technology, Fetscherstrasse 74, 01307 Dresden, Germany, Phone: +49 351 458 4166, Fax: +49 351 458 4304

References

[1] Basole A, White LE, Fitzpatrick D. Mapping multiple features in the population response of visual cortex. Nature 2003; 423: 986–990. Search in Google Scholar

[2] Bonhoeffer T, Kim D-S, Malonek D, Shoham D, Grinvald A. Optical imaging of the layout of functional domains in area 17 and across the area 17/18 border in cat visual cortex. Eur J Neurosci 1995; 7: 1973–1988. Search in Google Scholar

[3] Cao Y, Cai Z, Shen E, et al. Quantitative analysis of brain optical images with 2D C0 complexity measure. J Neurosci Methods 2007; 159: 181–186. Search in Google Scholar

[4] Coenen VA, Krings T, Weidemann J, Spangenberg P, Gilsbach JM, Rohde V. Diffusion weighted imaging combined with intraoperative 3D-ultrasound and fMRI for the resection of an optic radiation cavernoma. Zentralbl Neurochir 2003; 64: 133–137. Search in Google Scholar

[5] Curatolo JM, Macdonell RAL, Berkovic SF, Fabinyi GCA. Intraoperative monitoring to preserve central visual fields during occipital corticectomy for epilepsy. J Clin Neurosci 2000; 7: 234–237. Search in Google Scholar

[6] Frostig RD, Lieke EE, Ts’o DY, Grinvald A. Cortical functional architecture and local coupling between neuronal activity and the microcirculation revealed by in vivo high-resolution optical imaging of intrinsic signals. Proc Natl Acad Sci USA 1990; 87: 6082–6086. Search in Google Scholar

[7] Godde B, Leonhardt R, Cords SM, Dinse HR. Plasticity of orientation preference maps in the visual cortex of adult cats. Proc Natl Acad Sci USA 2002; 99: 6352–6357. Search in Google Scholar

[8] Grinvald A, Lieke E, Frostig RD, Gilbert CD, Wiesel TN. Functional architecture of cortex revealed by optical imaging of intrinsic signals. Nature 1986; 324: 361–364. Search in Google Scholar

[9] Haglund MM, Ojemann GA, Hochman DW. Optical imaging of epileptiform and functional activity in human cerebral cortex. Nature 1992; 358: 668–671. Search in Google Scholar

[10] Haglund MM, Hochman DW. Optical imaging of epileptiform activity in human neocortex. Epilepsia 2004; 45 (Suppl 4): 43–47. Search in Google Scholar

[11] Hirsch J, Ruge MI, Kim KH, et al. An integrated functional magnetic resonance imaging procedure for preoperative mapping of cortical areas associated with tactile, motor, language, and visual functions. Neurosurgery 2000; 47: 711–721. Search in Google Scholar

[12] Hübener M, Shoham D, Grinvald A, Bonhoeffer T. Spatial relationships among three columnar systems in cat area 17. J Neurosci 1997; 17: 9270–9284. Search in Google Scholar

[13] Kammer T, Vorwerg M, Herrnberger B. Anisotropy in the visual cortex investigated by neuronavigated transcranial magnetic stimulation. Neuroimage 2007; 36: 313–321. Search in Google Scholar

[14] Kim DS, Matsuda Y, Ohki K, Ajima A, Tanaka S. Geometrical and topological relationships between multiple functional maps in cat primary visual cortex. Neuroreport 1999; 10: 2515–2522. Search in Google Scholar

[15] Kodama K, Goto T, Sato A, Sakai K, Tanaka Y, Hongo K. Standard and limitation of intraoperative monitoring of the visual evoked potential. Acta Neurochir 2010; 152: 643–648. Search in Google Scholar

[16] Lieke EE, Frostig RD, Arieli A, Ts’o DY, Hildesheim R, Grinvald A. Optical imaging of cortical activity: real-time imaging using extrinsic dye-signals and high resolution imaging based on slow intrinsic-signals. Annu Rev Physiol 1989; 51: 543–559. Search in Google Scholar

[17] Lu HD, Roe AW. Optical imaging of contrast response in Macaque monkey V1 and V2. Cereb Cortex 2007; 17: 2675–2695. Search in Google Scholar

[18] Malonek D, Dirnagl U, Lindauer U, Yamada K, Kanno I, Grinvald A. Vascular imprints of neuronal activity: relationships between the dynamics of cortical blood flow, oxygenation, and volume changes following sensory stimulation. Proc Natl Acad Sci USA 1997; 94: 14826–14831. Search in Google Scholar

[19] Meyer T, Sobottka SB, Kirsch M, et al. Intraoperative optical imaging of functional brain areas for improved image guided surgery. Biomed Tech 2013; 58: 225–236. Search in Google Scholar

[20] Nariai T, Sato K, Hirakawa K, et al. Imaging of somatotopic representation of sensory cortex with intrinsic optical signals as guides for brain tumor surgery. J Neurosurg 2005; 103: 414–423. Search in Google Scholar

[21] Odom JV, Bach M, Brigell M, et al. ISCEV standard for clinical visual evoked potentials (2009 update). Doc Ophthalmol 2010; 120: 111–119. Search in Google Scholar

[22] Oelschlägel M, Meyer T, Wahl H, et al. Evaluation of intraoperative optical imaging analysis methods by phantom and patient measurements. Biomed Tech 2013; 58: 257–267. Search in Google Scholar

[23] Pouratian N, Sheth SA, Martin NA, Toga AW. Shedding light on brain mapping: advances in human optical imaging. Trends Neurosci 2003; 26: 277–282. Search in Google Scholar

[24] Prakash N, Biag JD, Sheth SA, et al. Temporal profiles and 2-dimensional oxy-, deoxy-, and total-hemoglobin somatosensory maps in rat versus mouse cortex. Neuroimage 2007; 37 (Suppl 1): 27–36. Search in Google Scholar

[25] Prakash N, Uhlemann F, Sheth SA, Bookheimer S, Martin N, Toga AW. Current trends in intraoperative optical imaging for functional brain mapping and delineation of lesions of language cortex. Neuroimage 2009; 47 (Suppl 2): 116–126. Search in Google Scholar

[26] Sato K, Nariai T, Sasaki S, et al. Intraoperative intrinsic optical imaging of neuronal activity from subdivisions of the human primary somatosensory cortex. Cereb Cortex 2002; 12: 269–280. Search in Google Scholar

[27] Sato K, Nariai T, Tanaka Y, et al. Functional representation of the finger and face in the human somatosensory cortex: intraoperative intrinsic optical imaging. Neuroimage 2005; 25: 1292–1301. Search in Google Scholar

[28] Schwartz TH, Chen LM, Friedman RM, Spencer DD, Roe AW. Intraoperative optical imaging of human face cortical topography: a case study. Neuroreport 2004; 15: 1527–1531. Search in Google Scholar

[29] Shmuel A, Grinvald A. Coexistence of linear zones and pinwheels within orientation maps in cat visual cortex. Proc Natl Acad Sci USA 2000; 97: 5568–5573. Search in Google Scholar

[30] Sobottka SB, Steinmetz A, Schackert G. Neuronavigation – the gentle way of removing brain tumours. Onkologie 1997; 20: 362–370. Search in Google Scholar

[31] Sobottka SB, Bredow J, Beuthien-Baumann B, Reiss G, Schackert G, Steinmeier R. Comparison of functional brain PET images and intraoperative brain-mapping data using image guided surgery. Comput Aided Surg 2002; 7: 317–325. Search in Google Scholar

[32] Sobottka SB, Meyer T, Kirsch M, et al. Intraoperative optical imaging of blood volume changes can visualize functional activated brain areas during brain surgery. Biomed Tech 2013; 58: 225–236. Search in Google Scholar

[33] Sun GC, Chen XL, Zhao Y, et al. Intraoperative high-field magnetic resonance imaging combined with fiber tract neuronavigation-guided resection of cerebral lesions involving optic radiation. Neurosurgery 2011; 69: 1070–1084. Search in Google Scholar

[34] Tani T, Yokoi I, Ito M, Tanaka S, Komatsu H. Functional organization of the cat visual cortex in relation to the representation of a uniform surface. J Neurophysiol 2003; 89: 1112–1125. Search in Google Scholar

[35] Tharin S, Golby A. Functional brain mapping and its applications to neurosurgery. Neurosurgery 2007; 60: 185–201. Search in Google Scholar

[36] Thudium MO, Campos AR, Urbach H, Clusmann H. The basal temporal approach for mesial temporal surgery: sparing the Meyer loop with navigated diffusion tensor tractography. Neurosurgery 2010; 67: 385–390. Search in Google Scholar

[37] Ts’o DY, Roe AW, Gilbert CD. A hierarchy of the functional organization for color, form and disparity in primate visual area V2. Vision Res 2001; 41: 1333–1349. Search in Google Scholar

[38] Villringer A, Dirnagl U. Coupling of brain activity and cerebral blood flow: basis of functional neuroimaging. Cerebrovasc. Brain Metab Rev 1995; 7: 240–276. Search in Google Scholar

[39] Wang G, Ding S, Yunokuchi K. Representation of cardinal contour overlaps less with representation of nearby angles in cat visual cortex. J Neurophysiol 2003; 90: 3912–3920. Search in Google Scholar

Received: 2012-10-18
Accepted: 2013-1-15
Published Online: 2013-2-18
Published in Print: 2013-06-01

©2013 by Walter de Gruyter Berlin Boston