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MRI Magnetic Field Stimulates Rotational Sensors of the Brain

MRI Magnetic Field Stimulates Rotational Sensors of the Brain

MRI Magnetic Field Stimulates Rotational Sensors of the

Please cite this article in press as: Roberts et al., MRI Magnetic Field Stimulates Rotational Sensors of the Brain, Current Biology(2011), doi:10.1016/j.cub.2011.08.029Current Biology 21, 1–6, October 11, 2011 ª2011 Elsevier Ltd All rights reservedDOI 10.1016/j.cub.2011.08.029MRI Magnetic Field StimulatesRotational Sensors of the BrainReportDale C. Roberts, 1, * Vincenzo Marcelli, 7 Joseph S. Gillen, 2,8John P. Carey, 3 Charles C. Della Santina, 3,4and David S. Zee 1,3,5,61Department of Neurology2Department of Radiology3Department of Otolaryngology–Head and Neck Surgery4Department of Biomedical Engineering5Department of Neuroscience6Department of OphthalmologyJohns Hopkins University School of Medicine, Baltimore,MD 21287, USA7Department of Neuroscience, School of Medicine,‘‘Federico II’’ University of Naples, 80131 Naples, Italy8F.M. Kirby Research Center, Kennedy Krieger Institute,Baltimore, MD 21205, USASummaryVertigo in and around magnetic resonance imaging (MRI)machines has been noted for years [1, 2]. Several mechanismshave been suggested to explain these sensations [3,4], yet without direct, objective measures, the cause isunknown. We found that all of our healthy human subjectsdeveloped a robust nystagmus while simply lying in thestatic magnetic field of an MRI machine. Patients lackinglabyrinthine function did not. We use the pattern of eyemovements as a measure of vestibular stimulation to showthat the stimulation is static (continuous, proportional tostatic magnetic field strength, requiring neither head movementnor dynamic change in magnetic field strength) anddirectional (sensitive to magnetic field polarity and headorientation). Our calculations and geometric model suggestthat magnetic vestibular stimulation (MVS) derives from aLorentz force resulting from interaction between themagnetic field and naturally occurring ionic currents in thelabyrinthine endolymph fluid. This force pushes on the semicircularcanal cupula, leading to nystagmus. We emphasizethat the unique, dual role of endolymph in the delivery ofboth ionic current and fluid pressure, coupled with the cupula’sfunction as a pressure sensor, makes magnetic-fieldinducednystagmus and vertigo possible. Such effects couldconfound functional MRI studies of brain behavior,including resting-state brain activity.Results and DiscussionRecently, in a study of functional magnetic resonance imaging(MRI) of caloric-induced vestibular responses, the eyes ofsome subjects were noted to drift while simply lying in theMRI magnet bore [5]. Animals show behavioral and posturalchanges when exposed to strong magnetic fields [6, 7]. Thevestibular labyrinth is the likely target because after labyrinthectomy,the animals no longer show abnormal posturalresponses due to the fields [8]. The vestibulo-ocular reflex*Correspondence: dale.roberts@jhu.edu(VOR) links labyrinthine stimulation to eye movements. Headrotation in one direction leads to eye rotation in the other,ensuring stable vision during head motion. Here, we use thelink between vestibular stimulation and eye movements toinvestigate magnetic vestibular stimulation (MVS). Normally,labyrinthine stimulation produces nystagmus, an alternatingslow drift (slow phase) and fast resetting movement (quickphase) of the eyes. We used the direction and velocity ofthe slow phases of nystagmus as a measure of the pattern oflabyrinthine stimulation.Previously Proposed Mechanisms and a Rationalefor Investigating Their RoleGlover gives an overview and mathematical analysis of threecandidate mechanisms for MVS: electromagnetic induction(EMI), magnetic susceptibility (MS), and magnetohydrodynamics(MHD) during head movements [4]. EMI (due to Faraday’slaw of induction) is a voltage induced by a changingmagnetic field. Although the MRI magnetic field is static, oursubjects moved through the magnetic field gradient into theMRI bore, producing a change in field strength, and hencean EMI voltage, within the subject. Faster movement produceslarger EMI. When there is no movement, there is no EMI.To investigate EMI’s possible role in MVS, we placed a smallcoil of wire (‘‘search coil’’) near the ear to record EMI voltage.EMI was only present during subject table motion into or outof the MRI bore. When the subject lies still outside or insidethe MRI bore, the EMI voltage is zero. We plotted both theEMI voltage and eye movements to compare the amplitude,direction, and timing of the eye movements relative to theEMI voltage induced by movement through the magnetic field.If EMI is the mechanism of MVS, we would expect the EMIvoltage on the search coil and the slow-phase eye velocity(SPV) to be correlated. Similarly, the previously proposedMHD mechanism requires movement through the field, so itseffect should also be correlated with the EMI voltage.Magnetic susceptibility effects are static (require no movement),but they are not sensitive to magnetic field polarity, soreversing the field polarity relative to the subject’s head andobserving whether the slow phases change direction shouldreveal whether MS is the underlying mechanism.Subject DataWe placed ten healthy human subjects and two patients withno labyrinthine function in MRI machines with magnetic fieldstrengths of 3 and 7 T and measured eye movements with aninfrared video camera while the subjects lay still in darkness.No MRI scans were performed—only the static magnetic fieldwas present. Darkness is essential to an uncontaminated VORmeasurement, because visual cues are used by the brain tosuppress the unwanted nystagmus [9]. We chose our testconditions to address the physical properties of the proposedmechanisms. We varied the speed and direction of subjectmovement into the bore, the duration in the bore, and the staticfield strength.First, we confirmed that the labyrinth was necessary to elicitthe nystagmus by examining two patients who had bilateralacquired loss of labyrinthine function (verified with clinical

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