Functional and diffusion tensor magnetic resonance imaging of the sheep brain

BMC Veterinary Research

Seung-Schik Yoo¹  Hyungmin Kim²  Erin Purcell-Estabrook³  Lori Foley³  Michael Y. Park¹  Stephanie D. Lee¹  Wonhye Lee¹ 

[1] Department of Radiology, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA, USA;Center for Bionics, Korea Institute of Science and Technology, Seoul, Korea;Invasive Cardiovascular Experimental Laboratory, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA, USA

关键词: Tractography;    DTI;    fMRI;    Visual;    Sensorimotor;    Sheep;   

Others  :  1228771
DOI  :  10.1186/s12917-015-0581-8

 received in 2014-11-06, accepted in 2015-10-12,  发布年份 2015

【 摘 要 】

Background

An ovine model can cast great insight in translational neuroscientific research due to its large brain volume and distinct regional neuroanatomical structures. The present study examined the applicability of brain functional magnetic resonance imaging (fMRI) and diffusion tensor imaging (DTI) to sheep using a clinical MR scanner (3 tesla) with a head coil. The blood-oxygenation-level-dependent (BOLD) fMRI was performed on anesthetized sheep during the block-based presentation of external tactile and visual stimuli using gradient echo-planar-imaging (EPI) sequence.

Results

The individual as well as group-based data processing subsequently showed activation in the eloquent sensorimotor and visual areas. DTI was acquired using 26 differential magnetic gradient directions to derive directional fractional anisotropy (FA) and apparent diffusion coefficient (ADC) values from the brain. White matter tractography was also applied to reveal the macrostructure of the corticospinal tracts and optic radiations.

Conclusions

Utilization of fMRI and DTI along with anatomical MRI in the sheep brain could shed light on a broader use of an ovine model in the field of translational neuroscientific research targeting the brain.

【 授权许可】

   
2015 Lee et al.

【 图 表 】

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【 参考文献 】

• [1]Yoo S-S, Bystritsky A, Lee J-H, Zhang Y, Fischer K, Min B-K et al.. Focused ultrasound modulates region-specific brain activity. NeuroImage. 2011; 56(3):1267-1275.
• [2]Cohen ZR, Zaubermann J, Harnof S, Mardor Y, Nass D, Zadicario E et al.. Magnetic resonance imaging-guided focused ultrasound for thermal ablation in the brain: a feasibility study in a swine model. Neurosurgery. 2007; 60(4):593-600.
• [3]Boltze J, Förschler A, Nitzsche B, Waldmin D, Hoffmann A, Boltze CM et al.. Permanent middle cerebral artery occlusion in sheep: a novel large animal model of focal cerebral ischemia. J Cereb Blood Flow Metab. 2008; 28(12):1951-1964.
• [4]Stypulkowski PH, Stanslaski SR, Jensen RM, Denison TJ, Giftakis JE. Brain stimulation for epilepsy – local and remote modulation of network excitability. Brain Stimul. 2014; 7(3):350-358.
• [5]Van den Heuvel C, Blumbergs PC, Finnie JW, Manavis J, Jones NR, Reilly PL et al.. Upregulation of amyloid precursor protein messenger RNA in response to traumatic brain injury: an ovine head impact model. Exp Neurol. 1999; 159(2):441-450.
• [6]Elias WJ, Huss D, Voss T, Loomba J, Khaled M, Zadicario E et al.. A pilot study of focused ultrasound thalamotomy for essential tremor. N Engl J Med. 2013; 369(7):640-648.
• [7]Martin E, Jeanmonod D, Morel A, Zadicario E, Werner B. High-intensity focused ultrasound for noninvasive functional neurosurgery. Ann Neurol. 2009; 66(6):858-861.
• [8]Basser PJ, Mattiello J, LeBihan D. MR diffusion tensor spectroscopy and imaging. Biophys J. 1994; 66(1):259-267.
• [9]Pierpaoli C, Jezzard P, Basser PJ, Barnett A, Di Chiro G. Diffusion tensor MR imaging of the human brain. Radiology. 1996; 201(3):637-648.
• [10]Jellison BJ, Field AS, Medow J, Lazar M, Salamat MS, Alexander AL. Diffusion tensor imaging of cerebral white matter: a pictorial review of physics, fiber tract anatomy, and tumor imaging patterns. AJNR Am J Neuroradiol. 2004; 25(3):356-369.
• [11]Basser PJ, Pajevic S, Pierpaoli C, Duda J, Aldroubi A. In vivo fiber tractography using DT-MRI data. Magn Reson Med. 2000; 44(4):625-632.
• [12]Behrens TE, Berg HJ, Jbabdi S, Rushworth MF, Woolrich MW. Probabilistic diffusion tractography with multiple fibre orientations: What can we gain? NeuroImage. 2007; 34(1):144-155.
• [13]Jiang H, van Zijl PCM, Kim J, Pearlson GD, Mori S. DtiStudio: resource program for diffusion tensor computation and fiber bundle tracking. Comput Methods Programs Biomed. 2006; 81(2):106-116.
• [14]Assaf Y, Pasternak O. Diffusion tensor imaging (DTI)-based white matter mapping in brain research: a review. J Mol Neurosci. 2007; 34(1):51-61.
• [15]Heeger DJ, Ress D. What does fMRI tell us about neuronal activity? Nat Rev Neurosci. 2002; 3(2):142-151.
• [16]Rumple A, McMurray M, Johns J, Lauder J, Makam P, Radcliffe M et al.. 3-dimensional diffusion tensor imaging (DTI) atlas of the rat brain. PLoS ONE. 2013; 8(7):e67334.
• [17]Weber R, Ramos-Cabrer P, Wiedermann D, van Camp N, Hoehn M. A fully noninvasive and robust experimental protocol for longitudinal fMRI studies in the rat. NeuroImage. 2006; 29(4):1303-1310.
• [18]Ronen I, Kim K-H, Garwood M, Ugurbil K, Kim D-S. Conventional DTI vs. slow and fast diffusion tensors in cat visual cortex. Magn Reson Med. 2003; 49(5):785-790.
• [19]Jezzard P, Rauschecker JP, Malonek D. An in vivo model for functional MRI in cat visual cortex. Magn Reson Med. 1997; 38(5):699-705.
• [20]Lee S-H, Jahng G-H, Choe I-H, Choi C-B, Kim D-H, Kim H-Y. Neural pathway interference by retained acupuncture: a functional MRI study of a dog model of Parkinson’s disease. CNS Neurosci Ther. 2013; 19(8):585-595.
• [21]Jacqmot O, Van Thielen B, Fierens Y, Hammond M, Willekens I, Van Schuerbeek P et al.. Diffusion tensor imaging of white matter tracts in the dog brain. Anat Rec. 2013; 296(2):340-349.
• [22]Opdam HI, Federico P, Jackson GD, Buchanan J, Abbott DF, Fabinyi GC et al.. A sheep model for the study of focal epilepsy with concurrent intracranial EEG and functional MRI. Epilepsia. 2002; 43(8):779-787.
• [23]Hoffmann A, Stoffel MH, Nitzsche B, Lobsien D, Seeger J, Schneider H et al.. The ovine cerebral venous system: comparative anatomy, visualization, and implications for translational research. PLoS ONE. 2014; 9(4):e92990.
• [24]Belliveau JW, Kwong KK, Kennedy DN, Baker JR, Stern CE, Benson R et al.. Magnetic resonance imaging mapping of brain function. Human visual cortex. Invest Radiol. 1992; 27 Suppl 2:S59-65.
• [25]Bandettini PA, Wong EC, Hinks RS, Tikofsky RS, Hyde JS. Time course EPI of human brain function during task activation. Magn Reson Med. 1992; 25(2):390-397.
• [26]Blamire AM, Ogawa S, Ugurbil K, Rothman D, McCarthy G, Ellermann JM et al.. Dynamic mapping of the human visual cortex by high-speed magnetic resonance imaging. Proc Natl Acad Sci U S A. 1992; 89(22):11069-73.
• [27]Yetkin FZ, Mueller WM, Hammeke TA, Morris GL, Haughton VM. Functional magnetic resonance imaging mapping of the sensorimotor cortex with tactile stimulation. Neurosurgery. 1995; 36(5):921-925.
• [28]Lowe AS, Beech JS, Williams SCR. Small animal, whole brain fMRI: innocuous and nociceptive forepaw stimulation. NeuroImage. 2007; 35(2):719-728.
• [29]Fa Z, Zhang P, Huang F, Li P, Zhang R, Xu R et al.. Activity-induced manganese-dependent functional MRI of the rat visual cortex following intranasal manganese chloride administration. Neurosci Lett. 2010; 481(2):110-114.
• [30]You Y, Klistorner A, Thie J, Graham SL. Improving reproducibility of VEP recording in rats: electrodes, stimulus source and peak analysis. Doc Ophthalmol. 2011; 123(2):109-119.
• [31]Fuller A, Hetem RS, Meyer LCR, Maloney SK. Angularis oculi vein blood flow modulates the magnitude but not the control of selective brain cooling in sheep. Am J Physiol Regul Integr Comp Physiol. 2011; 300(6):R1409-1417.
• [32]Mitchell J, Thomalla L, Mitchell G. Histological studies of the dorsal nasal, angularis oculi, and facial veins of sheep (Ovis aries). J Morphol. 1998; 237(3):275-281.
• [33]Simpson S, King JL. Localisation of the motor area in the sheep. Exp Physiol. 1911; 4(1):53-65.
• [34]Clarke PG, Whitteridge D. The cortical visual areas of the sheep. J Physiol. 1976; 256(3):497-508.
• [35]Alpert GF, Handwerker D, Sun FT, D’Esposito M, Knight RT. Spatio-temporal information analysis of event-related BOLD responses. NeuroImage. 2007; 34(4):1545-1561.
• [36]Hillman EMC. Coupling mechanism and significance of the BOLD signal: a status report. Annu Rev Neurosci. 2014; 37(1):161-181.
• [37]Wager TD, Vazquez A, Hernandez L, Noll DC. Accounting for nonlinear BOLD effects in fMRI: parameter estimates and a model for prediction in rapid event-related studies. NeuroImage. 2005; 25(1):206-218.
• [38]Shen Q, Ren H, Duong TQ. CBF, BOLD, CBV, and CMRO(2) fMRI signal temporal dynamics at 500-msec resolution. J Magn Reson Imaging. 2008; 27(3):599-606.
• [39]Yang Y, Gu H, Stein EA. Simultaneous MRI acquisition of blood volume, blood flow, and blood oxygenation information during brain activation. Magn Reson Med. 2004; 52(6):1407-1417.
• [40]Lahti KM, Ferris CF, Li F, Sotak CH, King JA. Comparison of evoked cortical activity in conscious and propofol-anesthetized rats using functional MRI. Magn Reson Med. 1999; 41(2):412-416.
• [41]Peeters RR, Tindemans I, De Schutter E, Van der Linden A. Comparing BOLD fMRI signal changes in the awake and anesthetized rat during electrical forepaw stimulation. Magn Reson Imaging. 2001; 19(6):821-826.
• [42]Tsurugizawa T, Uematsu A, Uneyama H, Torii K. Effects of isoflurane and alpha-chloralose anesthesia on BOLD fMRI responses to ingested L-glutamate in rats. Neuroscience. 2010; 165(1):244-251.
• [43]Booke M, Armstrong C, Hinder F, Conroy B, Traber LD, Traber DL. The effects of propofol on hemodynamics and renal blood flow in healthy and in septic sheep, and combined with fentanyl in septic sheep. Anesth Analg. 1996; 82(4):738-743.
• [44]Lin H-C, Purohit RC, Powe TA. Anesthesia in sheep with propofol or with xylazine-ketamine followed by halothane. Vet Surg. 1997; 26(3):247-252.
• [45]Myburgh JA, Upton RN, Grant C, Martinez A. Epinephrine, norepinephrine and dopamine infusions decrease propofol concentrations during continuous propofol infusion in an ovine model. Intensive Care Med. 2001; 27(1):276-282.
• [46]Brander A, Kataja A, Saastamoinen A, Ryymin P, Huhtala H, Öhman J et al.. Diffusion tensor imaging of the brain in a healthy adult population: Normative values and measurement reproducibility at 3 T and 1.5 T. Acta Radiol. 2010; 51(7):800-807.
• [47]Yarnykh VL, Yuan C. T1-insensitive flow suppression using quadruple inversion-recovery. Magn Reson Med. 2002; 48(5):899-905.
• [48]Morelli JN, Runge VM, Ai F, Attenberger U, Vu L, Schmeets SH et al.. An image-based approach to understanding the physics of MR artifacts. Radiographics. 2011; 31(3):849-866.
• [49]Matta BF, Heath KJ, Tipping K, Summors AC. Direct cerebral vasodilatory effects of sevoflurane and isoflurane. Anesthesiology. 1999; 91(3):677-680.
• [50]Reiz S, Bålfors E, Sørensen MB, Ariola S, Friedman A, Truedsson H. Isoflurane--a powerful coronary vasodilator in patients with coronary artery disease. Anesthesiology. 1983; 59(2):91-97.
• [51]Triantafyllou C, Hoge RD, Krueger G, Wiggins CJ, Potthast A, Wiggins GC et al.. Comparison of physiological noise at 1.5 T, 3 T and 7 T and optimization of fMRI acquisition parameters. NeuroImage. 2005; 26(1):243-250.
• [52]Friston KJ, Holmes AP, Worsley KJ. How many subjects constitute a study? NeuroImage. 1999; 10(1):1-5.
• [53]Forman SD, Cohen JD, Fitzgerald M, Eddy WF, Mintun MA, Noll DC. Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): use of a cluster-size threshold. Magn Reson Med. 1995; 33(5):636-647.
• [54]Song X-W, Dong Z-Y, Long X-Y, Li S-F, Zuo X-N, Zhu C-Z et al.. REST: A toolkit for resting-state functional magnetic resonance imaging data processing. PLoS ONE. 2011; 6(9):e25031.
• [55]Alexander AL, Lee JE, Lazar M, Field AS. Diffusion tensor imaging of the brain. Neurotherapeutics. 2007; 4(3):316-329.
• [56]Tournier JD, Calamante F, Connelly A. MRtrix: Diffusion tractography in crossing fiber regions. Int J Imaging Syst Technol. 2012; 22(1):53-66.
• [57]Farquharson S, Tournier JD, Calamante F, Fabinyi G, Schneider-Kolsky M, Jackson GD et al.. White matter fiber tractography: why we need to move beyond DTI. J Neurosurg. 2013; 118(6):1367-1377.