Advertisement
Original Investigation| Volume 23, ISSUE 2, P192-199, February 2016

Download started.

Ok

Evidence of Resting-state Activity in Propofol-anesthetized Patients with Intracranial Tumors

Published:November 25, 2015DOI:https://doi.org/10.1016/j.acra.2015.10.013

      Rationale and Objectives

      Resting-state (RS) networks, revealed by functional magnetic resonance imaging (fMRI) studies in healthy volunteers, have never been evaluated in anesthetized patients with brain tumors. Our purpose was to examine the presence of residual brain activity on the auditory network during propofol-induced loss of consciousness in patients with brain tumors.

      Materials and Methods

      Twenty subjects with intracranial masses were prospectively studied by means of intraoperative RS-fMRI acquisitions before any craniectomy. After performing single-subject independent component analysis, spatial maps and time courses were assigned to an auditory RS network template from the literature and compared via spatial regression coefficients.

      Results

      All fMRI data were of sufficient quality for further postprocessing. In all but two patients, the RS functional activity of the auditory network could be successfully mapped. In almost all patients, contralateral activation of the auditory network was present. No significant difference was found between the mean distance of the RS activity clusters and the lesion periphery for tumors located in the temporal gyri vs. those in other brain regions. The spatial deviation between the activated cluster in our experiment and the template was significantly (P = 0.04) higher in patients with tumors located in the temporal gyri than in patients with tumors located in other regions.

      Conclusions

      Propofol-induced anesthesia in patients with intracranial lesions does not alter the blood-oxygenation level-depended signal, and independent component analysis of intraoperative RS-fMRI may allow assessment of the auditory network in a clinical setting.

      Key Words

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Academic Radiology
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Gusnard D.A.
        • Raichle M.E.
        • Raichle M.E.
        Searching for a baseline: functional imaging and the resting human brain.
        Nat Rev Neurosci. 2001; 2: 685-694
        • Larson-Prior L.J.
        • Power J.D.
        • Vincent J.L.
        • et al.
        Modulation of the brain's functional network architecture in the transition from wake to sleep.
        Prog Brain Res. 2011; 193: 277-294
        • Fukunaga M.
        • Horovitz S.G.
        • van Gelderen P.
        • et al.
        Large-amplitude, spatially correlated fluctuations in BOLD fMRI signals during extended rest and early sleep stages.
        Magn Reson Imaging. 2006; 24: 979-992
        • Horovitz S.G.
        • Fukunaga M.
        • de Zwart J.A.
        • et al.
        Low frequency BOLD fluctuations during resting wakefulness and light sleep: a simultaneous EEG-fMRI study.
        Hum Brain Mapp. 2008; 29: 671-682
        • Greicius M.D.
        • Kiviniemi V.
        • Tervonen O.
        • et al.
        Persistent default-mode network connectivity during light sedation.
        Hum Brain Mapp. 2008; 29: 839-847
        • Horovitz S.G.
        • Braun A.R.
        • Carr W.S.
        • et al.
        Decoupling of the brain's default mode network during deep sleep.
        Proc Natl Acad Sci U S A. 2009; 106: 11376-11381
        • Boveroux P.
        • Vanhaudenhuyse A.
        • Bruno M.A.
        • et al.
        Breakdown of within- and between-network resting state functional magnetic resonance imaging connectivity during propofol-induced loss of consciousness.
        Anesthesiology. 2010; 113: 1038-1053
        • Peltier S.J.
        • Kerssens C.
        • Hamann S.B.
        • et al.
        Functional connectivity changes with concentration of sevoflurane anesthesia.
        Neuroreport. 2005; 16: 285-288
        • Vanhaudenhuyse A.
        • Noirhomme Q.
        • Tshibanda L.J.
        • et al.
        Default network connectivity reflects the level of consciousness in non-communicative brain-damaged patients.
        Brain. 2010; 133: 161-171
        • Boly M.
        • Tshibanda L.
        • Vanhaudenhuyse A.
        • et al.
        Functional connectivity in the default network during resting state is preserved in a vegetative but not in a brain dead patient.
        Hum Brain Mapp. 2009; 30: 2393-2400
        • Petersen K.D.
        • Landsfeldt U.
        • Cold G.E.
        • et al.
        Intracranial pressure and cerebral hemodynamic in patients with cerebral tumors: a randomized prospective study of patients subjected to craniotomy in propofol-fentanyl, isoflurane-fentanyl, or sevoflurane-fentanyl anesthesia.
        Anesthesiology. 2003; 98: 329-336
        • Damoiseaux J.S.
        • Rombouts S.A.
        • Barkhof F.
        • et al.
        Consistent resting-state networks across healthy subjects.
        Proc Natl Acad Sci U S A. 2006; 103: 13848-13853
        • Maudoux A.
        • Lefebvre P.
        • Cabay J.E.
        • et al.
        Auditory resting-state network connectivity in tinnitus: a functional MRI study.
        PLoS ONE. 2012; 7: e36222
        • Allen E.A.
        • Erhardt E.B.
        • Damaraju E.
        • et al.
        A baseline for the multivariate comparison of resting-state networks.
        Front Syst Neurosci. 2011; 5: 2
        • Kerssens C.
        • Hamann S.
        • Peltier S.
        • et al.
        Attenuated brain response to auditory word stimulation with sevoflurane: a functional magnetic resonance imaging study in humans.
        Anesthesiology. 2005; 103: 11-19
        • Veselis R.A.
        • Feshchenko V.A.
        • Reinsel R.A.
        • et al.
        Propofol and thiopental do not interfere with regional cerebral blood flow response at sedative concentrations.
        Anesthesiology. 2005; 102: 26-34
        • Chen X.
        • Xu B.N.
        • Meng X.
        • et al.
        Dual-room 1.5-T intraoperative magnetic resonance imaging suite with a movable magnet: implementation and preliminary experience.
        Neurosurg Rev. 2012; 35 (discussion 109-110): 95-109
        • Bell A.J.
        • Sejnowski T.J.
        An information-maximization approach to blind separation and blind deconvolution.
        Neural Comput. 1995; 7: 1129-1159
        • Holodny A.I.
        • Schulder M.
        • Liu W.C.
        • et al.
        The effect of brain tumors on BOLD functional MR imaging activation in the adjacent motor cortex: implications for image-guided neurosurgery.
        AJNR Am J Neuroradiol. 2000; 21: 1415-1422
        • Kokkonen S.M.
        • Kiviniemi V.
        • Makiranta M.
        • et al.
        Effect of brain surgery on auditory and motor cortex activation: a preliminary functional magnetic resonance imaging study.
        Neurosurgery. 2005; 57 (discussion 249–256): 249-256
        • Kokkonen S.M.
        • Nikkinen J.
        • Remes J.
        • et al.
        Preoperative localization of the sensorimotor area using independent component analysis of resting-state fMRI.
        Magn Reson Imaging. 2009; 27: 733-740
        • Zhang D.
        • Johnston J.M.
        • Fox M.D.
        • et al.
        Preoperative sensorimotor mapping in brain tumor patients using spontaneous fluctuations in neuronal activity imaged with functional magnetic resonance imaging: initial experience.
        Neurosurgery. 2009; 65: 226-236
        • Johnston A.J.
        • Steiner L.A.
        • Chatfield D.A.
        • et al.
        Effects of propofol on cerebral oxygenation and metabolism after head injury.
        Br J Anaesth. 2003; 91: 781-786
        • Heinke W.
        • Fiebach C.J.
        • Schwarzbauer C.
        • et al.
        Sequential effects of propofol on functional brain activation induced by auditory language processing: an event-related functional magnetic resonance imaging study.
        Br J Anaesth. 2004; 92: 641-650
        • Khalili-Mahani N.
        • van Osch M.J.
        • de Rooij M.D.
        • et al.
        Spatial heterogeneity of the relation between resting-state connectivity and blood flow: an important consideration for pharmacological studies.
        Hum Brain Mapp. 2014; 35: 929-942
        • Hou B.L.
        • Bradbury M.
        • Peck K.K.
        • et al.
        Effect of brain tumor neovasculature defined by rCBV on BOLD fMRI activation volume in the primary motor cortex.
        Neuroimage. 2006; 32: 489-497
        • Zou Q.
        • Wu C.W.
        • Stein E.A.
        • et al.
        Static and dynamic characteristics of cerebral blood flow during the resting state.
        Neuroimage. 2009; 48: 515-524
        • Qiu M.
        • Ramani R.
        • Swetye M.
        • et al.
        Anesthetic effects on regional CBF, BOLD, and the coupling between task-induced changes in CBF and BOLD: an fMRI study in normal human subjects.
        Magn Reson Med. 2008; 60: 987-996
        • Quigley M.
        • Cordes D.
        • Wendt G.
        • et al.
        Effect of focal and nonfocal cerebral lesions on functional connectivity studied with MR imaging.
        AJNR Am J Neuroradiol. 2001; 22: 294-300
        • Fukunaga M.
        • Horovitz S.G.
        • de Zwart J.A.
        • et al.
        Metabolic origin of BOLD signal fluctuations in the absence of stimuli.
        J Cereb Blood Flow Metab. 2008; 28: 1377-1387
        • Shulman R.G.
        • Rothman D.L.
        • Hyder F.
        Stimulated changes in localized cerebral energy consumption under anesthesia.
        Proc Natl Acad Sci U S A. 1999; 96: 3245-3250
        • Feldman S.C.
        • Chu D.
        • Schulder M.
        • et al.
        The blood oxygen level-dependent functional MR imaging signal can be used to identify brain tumors and distinguish them from normal tissue.
        AJNR Am J Neuroradiol. 2009; 30: 389-395
        • Dagli M.S.
        • Ingeholm J.E.
        • Haxby J.V.
        Localization of cardiac-induced signal change in fMRI.
        Neuroimage. 1999; 9: 407-415
        • van de Ven V.G.
        • Formisano E.
        • Prvulovic D.
        • et al.
        Functional connectivity as revealed by spatial independent component analysis of fMRI measurements during rest.
        Hum Brain Mapp. 2004; 22: 165-178
        • Kollndorfer K.
        • Fischmeister F.P.
        • Kasprian G.
        • et al.
        A systematic investigation of the invariance of resting-state network patterns: is resting-state fMRI ready for pre-surgical planning?.
        Front Hum Neurosci. 2013; 7: 95
        • Tie Y.
        • Rigolo L.
        • Norton I.H.
        • et al.
        Defining language networks from resting-state fMRI for surgical planning—a feasibility study.
        Hum Brain Mapp. 2014; 35: 1018-1030
        • Ma L.
        • Wang B.
        • Chen X.
        • et al.
        Detecting functional connectivity in the resting brain: a comparison between ICA and CCA.
        Magn Reson Imaging. 2007; 25: 47-56
        • van den Heuvel M.P.
        • Hulshoff Pol H.E.
        Exploring the brain network: a review on resting-state fMRI functional connectivity.
        Eur Neuropsychopharmacol. 2010; 20: 519-534
        • Cole D.M.
        • Smith S.M.
        • Beckmann C.F.
        Advances and pitfalls in the analysis and interpretation of resting-state FMRI data.
        Front Syst Neurosci. 2010; 4: 8
        • Soddu A.
        • Vanhaudenhuyse A.
        • Bahri M.A.
        • et al.
        Identifying the default-mode component in spatial IC analyses of patients with disorders of consciousness.
        Hum Brain Mapp. 2012; 33: 778-796