Abstract Nonhuman primates are important animal models in neuroscience research, which can be compatible with a variety of invasive and non-invasive methods of neural signal detection and neural activity regulation. Combined with the non-invasive method of non-human primate neuroscience research results, it is helpful for the clinical transformation of a large number of basic research results based on animal models. Among them,magnetic resonance (MR) brain imaging technology is the most important non-invasive detection method of brain nerve signal. The research ofmagnetic resonance imaging (MRI) in non-human primates plays an important role in understanding the physiological mechanism ofMRI, the research and development of quantitative physiological detection technology based on MRI, basic research of neuroscience, psychology and clinical pathological mechanism. But non-human primate MRI is facing many technical challenges, including the lack of appropriate MRI scanners and matching imaging hardware, the need for higher imaging resolution, and the compatibility of the needs of diverse animal experiments. Ultra-high field (UHF, field strength>3 T) MRI has the advantages of high signal-to-noise ratio, highblood oxygen level dependent (BOLD) signal detection sensitivity and submillimeter level high-resolution imaging ability, which is widely used in the brain imaging research of non-human primates. In this paper, we reviewed the application of UHF MR brain imaging in non-human primates, the technical challenges faced, and the current technical solutions. Finally, the advantages and limitations of the current methods were summarized and the development trend was proposed.
Xu Bin,Gao Yang,Roe Anna Wang, et al. Non-Human Primate Brain Imaging Technology at Ultra-High Field Magnetic Resonance Imaging[J]. Chinese Journal of Biomedical Engineering, 2021, 40(4): 469-476.
[1] Chen Gang, Wang Feng, Dillenburger BC, et al. Functional magnetic resonance imaging of awake monkeys: Some approaches for improving imaging quality[J]. Magnetic Resonance Imaging, 2012, 30(1): 36-47. [2] Öngür D, Price JL. The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans [J]. Cerebral Cortex, 2000, 10(3): 206-219. [3] Chudasama Y, Robbins TW. Functions of frontostriatal systems in cognition: comparative neuropsychopharmacological studies in rats, monkeys and humans [J]. Biological Psychology, 2006, 73(1): 19-38. [4] Lv Qian, Yang Liqin, Li Guoliang, et al. Large-scale persistent network reconfiguration induced by ketamine in anesthetized monkeys: relevance to mood disorders[J]. Biological Psychiatry, 2016, 79(9): 765-775. [5] Orban GA. Functional MRI in the awake monkey: The missing link [J]. Journal of Cognitive Neuroscience, 2002, 14(6): 965-969. [6] Wang Jiaojian, Zuo Zzhentao, Xie Sangma, et al. Parcellation of macaque cortex with anatomical connectivity profiles [J]. Brain Topography, 2018, 31(2): 161-173. [7] Zitella LM, Xiao Yizi, Teplitzky BA, et al. In vivo 7 T MRI of the non-human primate brainstem [J]. PLoS ONE, 2015, 10(5): 1-18. [8] 左真涛,张献昌,薛蓉. 人脑默认网络方向图:基于7 T fMRI的动态因果模型[J]. 生物化学与生物物理进展,2018, 45(5): 536-543. [9] Cho KH, Huang SM, Choi CH, et al. Development, integration and use of an ultrahigh-strength gradient system on a human-size 3 T magnet for small animal MRI [J]. PLoS ONE, 2019, 14(6): 1-18. [10] Ugurbil K. Magnetic resonance imaging at ultrahigh fields [J]. IEEE Transactions on Biomedical Engineering, 2014, 61(5): 1364-1379. [11] Wang Pinyi, Wang Dingxin, Zhang Jialu, et al. Evaluation of submillimeter diffusion imaging of the macaque brain using [J]. IEEE Transactions on Biomedical Engineering, 2019, 66(10): 2945-2951. [12] Metzger GJ, Van De Moortele PF, Akgun C, et al. Performance of external and internal coil configurations for prostate investigations at 7 T [J]. Magnetic Resonance in Medicine, 2010, 64(6): 1625-1639. [13] Wu Bing, Zhang Xiaoliang, Wang Chunsheng, et al. Flexible transceiver array for ultrahigh field human MR imaging [J]. Magnetic Resonance in Medicine, 2012, 68(4): 1332-1338. [14] 黄绮华,辛学刚,高 勇. 高场和超高场MR下人体内B1 场均匀性及SAR 随场强变化规律的研究[J]. 中国生物医学工程学报, 2013, 32(1): 22-27. [15] Lohrke J, Frenzel T, Endrikat J, et al. 25 years of contrast-enhanced MRI: Developments, current challenges and future perspectives [J]. Advances in Therapy, 2016, 33(1): 1-28. [16] Arcaro MJ, Pinsk MA, Li Xin, et al. Visuotopic organization of macaque posterior parietal cortex: A functional magnetic resonance imaging study[J]. Journal of Neuroscience, 2011, 31(6): 2064-2078. [17] Vanduffel W, Farivar R. Functional MRI of awake behaving macaques using standard equipment [M]. New York: Intechopen, 2014: 145-165. [18] Duyn JH. The future of ultra-high field MRI and fMRI for study of the human brain [J]. Neuroimage, 2012, 62(2): 1241-1248. [19] Winkler SA, Schmitt F, Landes H, et al. Gradient and shim technologies for ultra high field MRI [J]. Neuroimage, 2018, 168(3): 59-70. [20] Duong TQ, Kim D,Ugˇurbil K, et al. Spatiotemporal dynamics of the bold fMRI signals: Toward mapping submillimeter cortical columns using the early negative response [J]. Magnetic Resonance in Medicine, 2000, 44(2): 231-242. [21] Gilbert KM, Gati JS, Barker K, et al. Optimized parallel transmit and receive radiofrequency coil for ultrahigh-field MRI of monkeys [J]. Neuroimage, 2016, 125(48): 153-161. [22] Gilbert KM, Schaeffer DJ, Zeman P, et al. Concentric radiofrequency arrays to increase the statistical power of resting-state maps in monkeys [J]. Neuroimage, 2018, 178(57): 287-294. [23] Adriany G, Harel N, Yacoub E. 21 channel transceiver array for non-human primate applications at 7 tesla [C]// The 18th Annual Meeting of ISMRM. Stockholm: ISMRM, 2010:1490-1490. [24] Logothetis NK, Merkle H, Augath M, et al. Ultra high-resolution fMRI in monkeys with implanted RFcoils [J]. Neuron, 2002, 35(2): 227-242. [25] Gao Yang, Chen Weidao, Zhang Xiaotong. Investigating the influence of spatial constraints on ultimate receive coil performance for monkey brain MRI at 7 T [J]. IEEE Transactions on Medical Imaging, 2018, 37(7): 1723-1732. [26] Raaijmakers AJE, Luijten PR, Van Den Berg CAT. Dipole antennas for ultrahigh-field body imaging: A comparison with loop coils [j]. NMR in Biomedicine, 2016, 29(9): 1122-1130. [27] Yan Xinqiang, Wei Long, Xue Rong, et al. Hybrid monopole/loop coil array for human head mr imaging at 7 T [J]. Applied Magnetic Resonance, 2015, 46(5): 541-550. [28] Stockmann JP, Wald LL. In vivo B0 field shimming methods for mri at 7 T [J]. Neuroimage, 2018, 168(5): 71-87. [29] Stehling M, Turner Rr, Mansfield P. Echo-planar imaging: Magnetic resonance imaging in a fraction of a second [J]. Science, 1991, 254(5028): 43-50. [30] Wilson JL, Jenkinson M, Jezzard P. Optimization of static field homogeneity in human brain using diamagnetic passive shims [J]. Magnetic Resonance in Medicine, 2002, 48(5): 906-914. [31] Koch KM, Sacolick LI, Nixon TW, et al. Dynamically shimmed multivoxel 1 h magnetic resonance spectroscopy and multislice magnetic resonance spectroscopic imaging of the human brain [J]. Magnetic Resonance in Medicine, 2007, 57(3): 587-591. [32] Juchem C, Brown PB, Nixon TW, et al. Multicoil shimming of the mouse brain [J]. Magnetic Resonance in Medicine, 2011, 66(3): 893-900. [33] Juchem C, Nixon TW, Mcintyre S, et al. Dynamic multi-coil shimming of the human brain at 7 T [J]. Journal of Magnetic Resonance, 2011, 212(2): 280-288. [34] Gao Yang, Mareyam A, Sun Yi, et al. A 16-channel AC/DC array coil for anesthetized monkey whole-brain imaging at 7 T [J]. Neuroimage, 2020, 207: 1-11. [35] Cohen-Adad J, Tisdall MD, Kimmlingen R, et al. Improved Q-ball imaging using a 300 mT/m human gradient[C]// The 20th Annual Meeting of ISMRM. Melbourne: ISMRM, 2012: 4055-4055. [36] Tan ET, Lee SK, Weavers PT, et al. High slew-rate head-only gradient for improving distortion in echo planar imaging: Preliminary experience [J]. Journal of Magnetic Resonance Imaging, 2016, 44(3): 653-664. [37] Weavers PT, Shu YunHong, Tao Shengzhen, et al. Technical note: Compact three-tesla magnetic resonance imager with high-performance gradients passes acr image quality and acoustic noise tests [J]. Medical Physics, 2016, 43(3): 1259-1264. [38] Handler WB, Harris CT, Scholl TJ, et al. New head gradient coil design and construction techniques[J]. Journal of Magnetic Resonance Imaging, 2014, 39(5): 1088-1095. [39] Tang Fangfang, Liu Feng, Freschi F, et al. An improved asymmetric gradient coil design for high-resolution MRI head imaging [J]. Physics in Medicine and Biology, 2016, 61(24): 8875-8889. [40] Wade TP, Alejski A, Bartha J, et al. Design, construction and initial evaluation of a folded insertable head gradient coil[C]// The 22nd Annual Meeting of ISMRM. Milano: ISMRM, 2014:4851-4851. [41] Tomasi D, Xavier RF, Foerster B, et al. Asymmetrical gradient coil for head imaging [J]. Magnetic Resonance in Medicine, 2002, 48(4): 707-714. [42] Hodge MR, Horton W, Brown T, et al. Connectomedb—sharing human brain connectivity data [T]. Neuroimage, 2016, 124(10): 1102-1107. [43] Logothetis NK, Pauls J, Augath M, et al. Neurophysiological investigation of the basis of the fmri signal [j]. Nature, 2001, 412(6843): 150-157. [44] Chernov M, Roe AW. Infrared neural stimulation: A new stimulation tool for central nervous system applications [J]. Neurophotonics, 2014, 1(1): 1-8. [45] Roe AW, Chernov MM, Friedman RM, et al. In vivo mapping of cortical columnar networks in the monkey with focal electrical and optical stimulation [J]. Frontiers in Neuroanatomy, 2015, 9: 1-11. [46] Deffieux T, Demene C, Pernot M, et al. Functional ultrasound neuroimaging: A review of the preclinical and clinical state of the art [J]. Current Opinion in Neurobiology, 2018, 50(1): 128-135. [47] Leong ATL, Dong CM, Gao PP, et al. Optogenetic auditory fMRI reveals the effects of visual cortical inputs on auditory midbrain response [J]. Scientific Reports, 2018, 8(1): 1-11. [48] Gao Yang, Wang Pinyi, Qian Meizhen, et al. A surface loop array for in vivo small animal MRI/fMRI on 7 T human scanners [J]. Physics in Medicine and Biology, 2019, 64(3): 1-9. [49] Zhang Xiaotong, Zhang Jialu, Gao Yang, et al. A 16-channel dense array for in vivo animal cortical MRI/fMRI on 7 T human scanners [J]. IEEE Transactions on Biomedical Engineering, 2021,68: 1611-1618. [50] Quan Zhiyan, Gao Yang, Qu Shuxian, et al. A 16-channel loop array for in vivo macaque whole-brain imaging at 3 T [J]. Magnetic Resonance Imaging, 2020, 68: 167-172. [51] Allen PJ, Josephs O, Turner R. A method for removing imaging artifact from continuous EEG recorded during functional MRI [J]. NeuroImage, 2000, 12(2): 230-239. [52] Tyler WJ, Tufail Y, Finsterwald M, et al. Remote excitation of neuronal circuits using low-intensity, low-frequency ultrasound [J]. PLoS ONE, 2008, 3(10): 1-11. [53] Tufail Y, Matyushov A, Baldwin N, et al. Transcranial pulsed ultrasound stimulates intact brain circuits [J]. Neuron, 2010, 66(5): 681-694. [54] Yoo SS, Bystritsky A, Lee JH, et al. Focused ultrasound modulates region-specific brain activity [J]. NeuroImage, 2011, 56(3): 1267-1275. [55] Deffieux T, Younan Y, Wattiez N, et al. Low-intensity focused ultrasound modulates monkey visuomotor behavior [J]. Current Biology, 2013, 23: 2430-2433. [56] Legon W, Sato TF, Opitz A, et al. Transcranial focused ultrasound modulates the activity of primary somatosensory cortex in humans[J]. Nature Neuroscience, 2014, 17(2): 322-329. [57] Lee JH, Durand R, Gradinaru V, et al. Global and local fMRI signals driven by neurons defined optogenetically by type and wiring [J]. Nature, 2010, 465(7299): 788-792. [58] Lothet EH, Shaw KM, Lu H, et al. Selective inhibition of small-diameter axons using infrared light [J]. Scientific Reports, 2017, 7(1): 1-8. [59] Cayce JM, Friedman RM, Chen Gang, et al. Infrared neural stimulation of primary visual cortex in non-human primates[J]. NeuroImage, 2014, 84(40): 181-190. [60] Cayce JM, Friedman RM, Jansen ED, et al. Pulsed infrared light alters neural activity in rat somatosensory cortex in vivo [J]. NeuroImage, 2011, 57(1): 155-166. [61] Shapiro MG, Homma K, Villarreal S, et al. Infrared light excites cells by changing their electrical capacitance [J]. Nature Communications, 2012, 3(726): 1-10. [62] Wells J, Kao C, Jansen ED, et al. Application of infrared light for in vivo neural stimulation[J]. Journal of Biomedical Optics, 2005, 10(6): 1-12. [63] Kaas JH, Gharbawie OA, Stepniewska I. Cortical networks for ethologically relevant behaviors in primates [J]. American Journal of Primatology, 2013, 75(5): 407-414. [64] Brock AA, Friedman RM, Fan RH, et al. Optical imaging of cortical networks via intracortical microstimulation[J]. Journal of Neurophysiology, 2013, 110(11): 2670-2678. [65] Xu AG, Qian Meizhen, Tian Feiyan, et al. Focal infrared neural stimulation with high-field functional MRI: A rapid way to map mesoscale brain connectomes [J]. Science Advances, 2019, 5(4): 1-9. [66] Shi Sunhang, Xu AG, Rui Yun-Yun, et al. Infrared neural stimulation with 7T fMRI: A rapid in vivo method for mapping cortical connections of primate amygdala [J]. NeuroImage, 2021, 2021: 117818.
