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Short- and long-term effects of 3.5–23.0 Tesla ultra-high magnetic fields on mice behaviour

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Abstract

Objectives

Higher static magnetic field (SMF) enables higher imaging capability in magnetic resonance imaging (MRI), which encourages the development of ultra-high field MRIs above 20 T with a prerequisite for safety issues. However, animal tests of ≥ 20 T SMF exposure are very limited. The objective of the current study is to evaluate mice behaviour consequences of 3.5–23.0 T SMF exposure.

Methods

We systematically examined 112 mice for their short- and long-term behaviour responses to a 2-h exposure of 3.5–23.0 T SMFs. Locomotor activity and cognitive functions were measured by five behaviour tests, including balance beam, open field, elevated plus maze, three-chamber social recognition, and Morris water maze tests.

Results

Besides the transient short-term impairment of the sense of balance and locomotor activity, the 3.5–23.0 T SMFs did not have long-term negative effects on mice locomotion, anxiety level, social behaviour, or memory. In contrast, we observed anxiolytic effects and positive effects on social and spatial memory of SMFs, which is likely correlated with the significantly increased CaMKII level in the hippocampus region of high SMF-treated mice.

Conclusions

Our study showed that the short exposures to high-field SMFs up to 23.0 T have negligible side effects on healthy mice and may even have beneficial outcomes in mice mood and memory, which is pertinent to the future medical application of ultra-high field SMFs in MRIs and beyond.

Key Points

• Short-term exposure to magnetic fields up to 23.0 T is safe for mice.

• High-field static magnetic field exposure transiently reduced mice locomotion.

• High-field static magnetic field enhances memory while reduces the anxiety level.

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Abbreviations

Arc:

Apoptosis repressor with CARD

CaMKII:

Ca2+/calmodulin-dependent protein kinase II

cm/sec:

Average velocity

EPM:

Elevated plus maze

GAPDH:

Glyceraldehyde-3-phosphate dehydrogenase

IOD:

Integrated optical density

MRI:

Magnetic resonance imaging

MWM:

Morris water maze

NMDAR1:

N-Methyl-d-aspartate receptor subunit 1

OFT:

Open field test

SDS:

Sodium dodecyl sulfate

SMF:

Static magnetic field

T:

Unit of magnetic field intensity: Tesla

TBST:

Tris-buffered saline with Tween

TMS:

Transcranial magnetic stimulation

UHF-MRI:

Ultra-high field MRI

USTC:

University of Science and Technology of China

References

  1. Polimeni JR, Uludağ K (2018) Neuroimaging with ultra-high field MRI: present and future. Neuroimage 168:1–6

  2. Ugurbil K, Garwood M, Moortele PF et al (2006) 9.4 T human MRI: preliminary results. Magn Reson Med 56(6):1274–1282

    Article  Google Scholar 

  3. Henning A, Graaf R, Feyter H et al (2021) Deuterium metabolic imaging in the human brain at 9.4 Tesla with high spatial and temporal resolution. Neuroimage 244(1):118639

  4. Nowogrodzki A (2018) The world’s strongest MRI machines are pushing human imaging to new limits. Nature 563(7729):24–26

    Article  CAS  Google Scholar 

  5. Nagel AM, Umathum R, Rösler MB et al (2016) (39) K and (23) Na relaxation times and MRI of rat head at 21.1 T. NMR Biomed 29(6):759–766

    Article  Google Scholar 

  6. Schepkin VD, Bejarano FC, Morgan T, Gower-Winter S, Ozambela M Jr, Levenson CW (2012) In vivo magnetic resonance imaging of sodium and diffusion in rat glioma at 21.1 T. Magn Reson Med 67(4):1159–1166

    Article  CAS  Google Scholar 

  7. Budinger TF, Bird MD (2018) MRI and MRS of the human brain at magnetic fields of 14T to 20T: technical feasibility, safety, and neuroscience horizons. Neuroimage 168:509–531

  8. Tian X, Wang Z, Zhang L et al (2018) Effects of 3.7 T-24.5 T high magnetic fields on tumor-bearing mice. Chinese Phys B 27(11):118703

    Article  CAS  Google Scholar 

  9. Tian X, Lv Y, Fan Y, et al (2020) Safety evaluation of mice exposed to 7.0–33.0 T high static magnetic fields. J Magn Reson Imaging. https://doi.org/10.1002/jmri.27496.

  10. Tian X, Wang D, Feng S et al (2019) Effects of 3.5-23.0 T static magnetic fields on mice: a safety study. Neuroimage 199:273–280

  11. Silverman JL, Yang M, Lord C, Crawley JN (2010) Behavioural phenotyping assays for mouse models of autism. Nat Rev Neurosci 11(7):490–502

    Article  CAS  Google Scholar 

  12. Hsiao EY, McBride SW, Hsien S et al (2013) Microbiota modulate behavioral and physiological abnormalities associated with neurodevelopmental disorders. Cell 155(7):1451–1463

    Article  CAS  Google Scholar 

  13. Semple BD, Canchola SA, Noble-Haeusslein LJ (2012) Deficits in social behavior emerge during development after pediatric traumatic brain injury in mice. J Neurot 29(17):2672–2683

    Article  Google Scholar 

  14. Crawley JN (2004) Designing mouse behavioral tasks relevant to autistic-like behaviors. Ment Retard Dev D R 10(4):248–258

    Article  Google Scholar 

  15. Gonzales EL, Yang SM, Choi CS et al (2015) Repeated neonatal propofol administration induces sex-dependent long-term impairments on spatial and recognition memory in rats. Biomol Ther 23(3):251–260

    Article  CAS  Google Scholar 

  16. Mayford M, Bach ME, Huang YY, Wang L, Hawkins RD, Kandel ER (1996) Control of memory formation through regulated expression of a CaMKII transgene. Science 274(5293):1678–1683

    Article  CAS  Google Scholar 

  17. Zalcman G, Federman N, Romano A (2018) CaMKII isoforms in learning and memory: localization and function. Front Mol Neurosci 11:445

    Article  CAS  Google Scholar 

  18. Ward B, Zee D (2016) Dizziness and vertigo during MRI. New Engl J Med 375(21):e44

    Article  Google Scholar 

  19. Schaap K, Christopher-de Vries Y, Mason CK, de Vocht F, Portengen L, Kromhout H (2014) Occupational exposure of healthcare and research staff to static magnetic stray fields from 1.5-7 Tesla MRI scanners is associated with reporting of transient symptoms. Occup Environ Med 71(6):423–429

    Article  Google Scholar 

  20. Schaap K, Portengen L, Kromhout H (2016) Exposure to MRI-related magnetic fields and vertigo in MRI workers. Occup Environ Med 73(3):161–166

    Article  Google Scholar 

  21. Pais-Roldán P, Singh AP, Schulz H, Yu X (2016) High magnetic field induced otolith fusion in the zebrafish larvae. Sci Rep 6:24151

    Article  Google Scholar 

  22. Roberts DC, Marcelli V, Gillen JS, Carey JP, Della Santina CC, Zee DS (2011) MRI magnetic field stimulates rotational sensors of the brain. Curr Biol 21(19):1635–1640

    Article  CAS  Google Scholar 

  23. Straumann D, Bockisch CJ (2011) Neurophysiology: vertigo in MRI machines. Curr Biol 21(19):R806–R807

    Article  CAS  Google Scholar 

  24. Houpt TA, Kwon B, Houpt CE, Neth B, Smith JC (2013) Orientation within a high magnetic field determines swimming direction and laterality of c-Fos induction in mice. Am J Phys Regul Integr Comp Phys 305(7):R793–R803

    CAS  Google Scholar 

  25. Tkáč I, Benneyworth MA, Nichols-Meade T et al (2021) Long-term behavioral effects observed in mice chronically exposed to static ultra-high magnetic fields. Magn Reson Med 86(3):1544–1559

    Article  Google Scholar 

  26. Reardon J, Solvason BH, Janicak PG et al (2007) Efficacy and safety of transcranial magnetic stimulation in the acute treatment of major depression: a multisite randomized controlled trial. Biol Psychiatry 62(11):1208–1216

    Article  Google Scholar 

  27. Zwanzger P, Steinberg C, Rehbein MA et al (2014) Inhibitory repetitive transcranial magnetic stimulation (rTMS) of the dorsolateral prefrontal cortex modulates early affective processing. Neuroimage 101:193–203

  28. Luber BM, Davis S, Bernhardt E et al (2017) Using neuroimaging to individualize TMS treatment for depression: toward a new paradigm for imaging-guided intervention. Neuroimage 148:1–7

  29. Pascual-Leone A, Rubio B, Pallardo F, Catala MD (1996) Rapid-rate transcranial magnetic stimulation of left dorsolateral prefrontal cortex in drug-resistant depression. Lancet 348(9022):233–237

    Article  CAS  Google Scholar 

  30. George MS, Wassermann EM, Williams WA et al (1995) Daily repetitive transcranial magnetic stimulation (rTMS) improves mood in depression. Neuroreport 6(14):1853–1856

  31. Pirmoradi M, Dolatshahi B, Rostami R, Mohammadkhani P, Dadkhah A (2017) The changes of social performance with transcranial magnetic stimulation (TMS) in depressed patients. Eur Psychiatry 41(S1):S375–S376

    Article  Google Scholar 

  32. Oliveira FT, Diedrichsen J, Verstynen T, Duque J, Ivry RB (2010) Transcranial magnetic stimulation of posterior parietal cortex affects decisions of hand choice. Proc Natl Acad Sci U S A 107(41):17751–17756

    Article  CAS  Google Scholar 

  33. Lv Y, Fan Y, Tian X, et al (2021). A 33 T The anti-depressive effects of ultra-high static magnetic field. J Magn Reson Imaging. https://doi.org/10.1002/jmri.28035

  34. Boerema AS, Heesterbeek M, Boersma SA et al (2018) Beneficial effects of whole body vibration on brain functions in mice and humans. Dose Response 16(4):1559325818811756

  35. Cason AM, Kwon B, Smith JC, Houpt, T. A. (2009) Labyrinthectomy abolishes the behavioral and neural response of rats to a high-strength static magnetic field. Physiol Behav 97(1): 36–43

  36. Wang S, Luo J, Lv H et al (2019) Safety of exposure to high static magnetic fields (2 T-12 T): a study on mice. Eur Radiol 29(11):6029–6037

    Article  Google Scholar 

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Acknowledgements

We would like to thank the staff members in the High Magnetic Field Laboratory, Chinese Academy of Sciences, for their technical assistance, and Shu-tong Maggie Wang for cartoon illustration.

Funding

This study has received funding from the National Key R&D Program of China (2016YFA0400900) to Xin Zhang and Tian Xue; National Natural Science Foundation of China (U21A20148), the CASHIPS Director’s Fund (BJPY2021A06, 2021YZGH04) to Xin Zhang; National Natural Science Foundation of China (52007185) to Xiaofei Tian; National Natural Science Foundation of China (U20A2017 and 32071020), Guangdong Basic and Applied Basic Research Foundation (2020B1515120014), and Shenzhen Key Laboratory of Drug Addiction (ZDSYS20190902093601675) to Jin Bao; and CAS Project for Young Scientists in Basic Research (YSBR-013) to Tian Xue and international collaboration grant (211134KYSB20190122) to Jin Bao.

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Author notes

  1. Md Hasanuzzaman Khan and Xinfeng Huang contributed equally to this work.

Authors and Affiliations

  1. Hefei National Laboratory for Physical Sciences at the Microscale, Neurodegenerative Disorder Research Center, CAS Key Laboratory of Brain Function and Disease, School of Life Sciences, Eye Center, The First Affiliated Hospital of USTC, Division of Life Sciences and Medicine, University of Science and Technology of China, Huangshan Road 443, Hefei, 230026, Anhui, China

    Md Hasanuzzaman Khan, Xinfeng Huang, Changjie Ouyang, Jutao Chen, Tian Xue & Jin Bao

  2. Institute of Physical Science and Information Technology, Anhui University, Hefei, 230601, Anhui, China

    Xiaofei Tian, Changjie Ouyang & Xin Zhang

  3. High Magnetic Field Laboratory, Key Laboratory of High Magnetic Field and Ion Beam Physical Biology, Hefei Institutes of Physical Science, Chinese Academy of Sciences, Shushanhu Road #350, Hefei, 230031, Anhui, China

    Xiaofei Tian, Dongmei Wang, Shuang Feng & Xin Zhang

  4. Shenzhen Neher Neural Plasticity Laboratory, the Brain Cognition and Brain Disease Institute, Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences (CAS); Shenzhen-Hong Kong Institute of Brain Science-Shenzhen Fundamental Research Institutions, Shenzhen, 518055, China

    Jin Bao

  5. International Magnetobiology Frontier Research Center, Science Island, Hefei, 230031, Anhui, China

    Xin Zhang

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  1. Md Hasanuzzaman Khan
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  8. Tian Xue
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  9. Jin Bao
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  10. Xin Zhang
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Corresponding authors

Correspondence to Tian Xue, Jin Bao or Xin Zhang.

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Guarantor

The scientific guarantor of this publication is Dr. Xin Zhang.

Conflict of interest

The authors of this manuscript declare no relationships with any companies whose products or services may be related to the subject matter of the article.

Statistics and biometry

One of the authors has significant statistical expertise.

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Approval from the institutional animal care committee was obtained.

Ethics approval

Institutional review board approval was obtained.

Study subjects or cohorts overlap

Some study subjects have been previously reported in Neuroimage. 2019. 199. 273-280.

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Khan, M.H., Huang, X., Tian, X. et al. Short- and long-term effects of 3.5–23.0 Tesla ultra-high magnetic fields on mice behaviour. Eur Radiol 32, 5596–5605 (2022). https://doi.org/10.1007/s00330-022-08677-8

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  • DOI: https://doi.org/10.1007/s00330-022-08677-8

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