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Title: Injury characteristics of the Papez circuit in patients with diffuse axonal injury: a diffusion tensor tractography study

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Abstract

We investigate the characteristics of injury of four portions of the Papez circuit in patients with diffuse axonal injury (DAI), using diffusion tensor tractography (DTT). Thirty-four consecutive patients with DAI and 30 normal control subjects were recruited. Four portions of the Papez circuit were reconstructed: the fornix, cingulum, thalamocingulate tract, and mammillothalamic tract. Analysis of DTT parameters [fractional anisotropy (FA) and tract volume (TV)] and configuration (narrowing, discontinuation, or non-reconstruction) was performed for each portion of the Papez circuit. The Memory Assessment Scale (MAS) was used for the estimation of cognitive function. In the group analysis, decreased fractional anisotropy and tract volume of the entire Papez circuit were observed in the patient group compared with the control group (p < 0.05). In the individual analysis, all four portions of the Papez circuit were injured in terms of DTT parameters or configuration. Positive correlation was observed between TV of the fornix and short-term memory on MAS r = 0.618, p < 0.05), and between FA of the fornix and total memory on MAS (r = 0.613, p < 0.05). We found that all four portions of the Papez circuit in the patient group were vulnerable to DAI, and among four portions of the Papez circuit, the fornix was the most vulnerable portion in terms of injury incidence and severity.

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References

  1. Papez JW (1995) A proposed mechanism of emotion (reprinted from archives of neurology and psychiatry, vol 38, pg 725, 1937). J Neuropsychiatry Clin Neurosci 7:103–112

    Article  PubMed  CAS  Google Scholar 

  2. Naganawa S, Sato C, Ishihra S, Kumada H, Ishigaki T, Miura S, Watanabe M, Maruyama K, Takizawa O (2004) Serial evaluation of diffusion tensor brain fiber tracking in a patient with severe diffuse axonal injury. AJNR Am J Neuroradiol 25:1553–1556

    PubMed  PubMed Central  Google Scholar 

  3. Choi SH, Kim YB, Paek SH, Cho ZH (2019) Papez circuit observed by in vivo human brain with 7.0T MRI super-resolution track density imaging and track tracing. Front Neuroanat 13:1–5

    Article  Google Scholar 

  4. Choi SH, Kim YB, Cho ZH (2018) Newly observed anterior thalamocortical fiber of the thalamus using 7.0 T super-resolution magnetic resonance tractography and its implications for the classical Papez circuit. J Neuroradiol 45:206–210

    Article  PubMed  Google Scholar 

  5. Wei PH, Mao ZQ, Cong F, Yeh FC, Wang B, Ling ZP, Liang SL, Chen L, Yu XG (2017) In Vivo visualization of connections among revised papez circuit hubs using full Q-space diffusion spectrum imaging tractography. Neuroscience 357:400–410

    Article  PubMed  CAS  Google Scholar 

  6. Ducreux D, Huynh I, Fillard P, Renoux J, Petit-Lacour MC, Marsot-Dupuch K, Lasjaunias P (2005) Brain MR diffusion tensor imaging and fibre tracking to differentiate between two diffuse axonal injuries. Neuroradiology 47:604–608

    Article  PubMed  CAS  Google Scholar 

  7. Sugiyama K, Kondo T, Higano S, Endo M, Watanabe H, Shindo K, Izumi SI (2007) Diffusion tensor imaging fiber tractography for evaluating diffuse axonal injury. Brain Inj 21:413–419

    Article  PubMed  Google Scholar 

  8. Xu J, Rasmussen IA, Lagopoulos J, Haberg A (2007) Diffuse axonal injury in severe traumatic brain injury visualized using high-resolution diffusion tensor imaging. J Neurotrauma 24:753–765

    Article  PubMed  Google Scholar 

  9. Wang JY, Bakhadirov K, Devous MD Sr, Abdi H, McColl R, Moore C, Marquez de la Plata CD, Ding K, Whittemore A, Babcock E, Rickbeil T, Dobervich J, Kroll D, Dao B, Mohindra N, Madden CJ, Diaz-Arrastia R (2008) Diffusion tensor tractography of traumatic diffuse axonal injury. Arch Neurol 65:619–626

    PubMed  Google Scholar 

  10. Kwon HG, Lee HD, Jang SH (2014) Injury of the mammillothalamic tract in patients with thalamic hemorrhage. Front Hum Neurosci 8:259

    PubMed  PubMed Central  Google Scholar 

  11. Sugiyama K, Kondo T, Oouchida Y, Suzukamo Y, Higano S, Endo M, Watanabe H, Shindo K, Izumi SI (2009) Clinical utility of diffusion tensor imaging for evaluating patients with diffuse axonal injury and cognitive disorders in the chronic stage. J Neurotrauma 26:1879–1890

    Article  PubMed  Google Scholar 

  12. Yang DS, Kwon HG, Jang SH (2016) Injury of the thalamocingulate tract in the papez circuit in patients with mild traumatic brain injury. Am J Phys Med Rehabil 95:e34–38

    Article  PubMed  Google Scholar 

  13. Gu L, Li J, Feng DF, Cheng ET, Li DC, Yang XQ, Wang BC (2013) Detection of white matter lesions in the acute stage of diffuse axonal injury predicts long-term cognitive impairments: a clinical diffusion tensor imaging study. J Trauma Acute Care Surg 74:242–247

    Article  PubMed  Google Scholar 

  14. Jang SH, Kim SH, Lee HD (2019) Traumatic axonal injury of the cingulum in patients with mild traumatic brain injury: a diffusion tensor tractography study. Neural Regen Res 14:1556–1561

    Article  PubMed  PubMed Central  Google Scholar 

  15. Jang SH, Kwon HG (2018) Injury of the Papez circuit in a patient with traumatic spinal cord injury and concomitant mild traumatic brain injury. Neural Regen Res 13:161–162

    Article  PubMed  PubMed Central  Google Scholar 

  16. Jang SH, Kwon HG (2016) Neural injury of the Papez circuit following hypoxic-ischemic brain injury a case report. Medicine 95:e5173

    Article  PubMed  PubMed Central  Google Scholar 

  17. Jang SH, Kwon HG (2017) Diffuse injury of the Papez circuit by focal head trauma: a diffusion tensor tractography study. Acta Neurol Belg 117:389–391

    Article  PubMed  Google Scholar 

  18. Jang SH, Yeo SS (2016) Injury of the Papez circuit in a patient with provoked confabulation following subarachnoid hemorrhage: a diffusion tensor tractography study. Acta Neurol Belg 116:655–658

    Article  PubMed  Google Scholar 

  19. Chang MC, Yeo SS, Do Lee H, Jang SH (2016) Diffusion tensor tractography in a patient with memory impairment following encephalitis. Acta Neurol Belg 116:629–631

    Article  PubMed  Google Scholar 

  20. Corrigan JD, Selassie AW, Orman JA (2010) The epidemiology of traumatic brain injury. J Head Trauma Rehabil 25:72–80

    Article  PubMed  Google Scholar 

  21. Adams JH, Graham DI, Murray LS, Scot G (1982) Diffuse axonal injury due to nonmissile head injury in humans: ananalysis of 45 cases. Ann Neurol 12:557–563

    Article  PubMed  CAS  Google Scholar 

  22. Meythaler JM, Peduzzi JD, Eleftheriou E, Novack TA (2001) Current concepts: diffuse axonal injury-associated traumatic brain injury. Arch Phys Med Rehabil 82:1461–1471

    Article  PubMed  CAS  Google Scholar 

  23. Scheid R, Walther KR, Guthke T, Preul C, von Cramon DY (2006) Cognitive sequelae of diffuse axonal injury. Arch Neurol 63:418–424

    Article  PubMed  Google Scholar 

  24. Gennarelli TA (1993) Cerebral concussion and diffuse brain injuries. In: Cooper PR (ed) Head injury, 3rd edn. Williams and Wilkins, Baltimore, pp 137–158

    Google Scholar 

  25. Adams JH, Doyle D, Ford I, Gennarelli TA, Graham DI, McLellan DR (1989) Diffuse axonal injury in head injury: definition, diagnosis and grading. Histopathology 15:49–59

    Article  PubMed  CAS  Google Scholar 

  26. Parizel PM, Ozsarlak O, Van Goethem JW, van den Hauwe L, Dillen C, Verlooy J, Cosyns P, De Schepper AM (1998) Imaging findings in diffuse axonal injury after closed head trauma. Eur Radiol 8:960–965

    Article  PubMed  CAS  Google Scholar 

  27. Smith SM, Jenkinson M, Woolrich MW, Beckmann CF, Behrens TEJ, Johansen-Berg H, Bannister PR, De Luca M, Drobnjak I, Flitney DE, Niazy RK, Saunders J, Vickers J, Zhang YY, De Stefano N, Brady JM, Matthews PM (2004) Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23:S208–S219

    Article  PubMed  Google Scholar 

  28. Mesulam MM (2004) The cholinergic innervation of the human cerebral cortex. Prog Brain Res 145:67–78

    Article  PubMed  Google Scholar 

  29. Williams JM (1991) Memory assessment scales. Psychologiccal Assessment Resources, Odessa, FL

    Google Scholar 

  30. Evans JD (1996) Straignt forward statistics for the behavioural science. Pacific Grove, CA

    Google Scholar 

  31. Assaf Y, Pasternak O (2008) Diffusion tensor imaging (DTI)-based white matter mapping in brain research: a review. J Mol Neurosci 34:51–61

    Article  PubMed  CAS  Google Scholar 

  32. Mori S, Crain BJ, Chacko VP, van Zijl PCM (1999) Three-dimensional tracking of axonal projections in the brain by magnetic resonance imaging. Ann Neurol 45:265–269

    Article  PubMed  CAS  Google Scholar 

  33. Neil JJ (2008) Diffusion imaging concepts for clinicians. J Magn Reson Imaging 27:1–7

    Article  PubMed  Google Scholar 

  34. Pagani E, Agosta F, Rocca MA, Caputo D, Filippi M (2008) Voxel-based analysis derived from fractional anisotropy images of white matter volume changes with aging. Neuroimage 41:657–667

    Article  PubMed  Google Scholar 

  35. Gentry LR, Godersky JC, Thompson B (1988) MR imaging of head trauma: review of the distribution and radiopathologic features of traumatic lesions. AJR Am J Roentgenol 150:663–672

    Article  PubMed  CAS  Google Scholar 

  36. Leclercq PD, McKenzie JE, Graham DI, Gentleman SM (2001) Axonal injury is accentuated in the caudal corpus callosum of head-injured patients. J Neurotrauma 18:1–9

    Article  PubMed  CAS  Google Scholar 

  37. Nieuwenhuys R, Voogd J, Cv H (2008) The human central nervous system. Springer, New York

    Book  Google Scholar 

  38. Hong JH, Jang SH (2010) Neural pathway from nucleus basalis of meynert passing through the cingulum in the human brain. Brain Res 1346:190–194

    Article  PubMed  CAS  Google Scholar 

  39. Yoo JS, Kim OL, Kim SH, Kim MS, Jang SH (2014) Relation between cognition and neural connection from injured cingulum to brainstem cholinergic nuclei in chronic patients with traumatic brain injury. Brain Inj 28:1257–1261

    Article  PubMed  Google Scholar 

  40. Parker GJM, Alexander DC (2005) Probabilistic anatomical connectivity derived from the microscopic persistent angular structure of cerebral tissue. Philos Trans R Soc Lond B Biol Sci 360:893–902

    Article  PubMed  PubMed Central  Google Scholar 

  41. De Bondt T, Van Hecke W, Veraart J, Leemans A, Sijbers J, Sunaert S, Jacquemyn Y, Parizel PM (2013) Does the use of hormonal contraceptives cause microstructural changes in cerebral white matter? Preliminary results of a DTI and tractography study. Eur Radiol 23:57–64

    Article  PubMed  Google Scholar 

Download references

Funding

This work was supported by the National Research Foundation (NRF) of Korea Grant funded by the Korean Government (MSIP) (2018R1A2B6000996).

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Authors and Affiliations

  1. Department of Physical Medicine and Rehabilitation, College of Medicine, Yeungnam University, 317-1, Daemyungdong, Namku, Taegu, 705-717, Republic of Korea

    Sung Ho Jang & You Sung Seo

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  1. Sung Ho Jang
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  2. You Sung Seo
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Contributions

Sung Ho Jang: study concept and design, manuscript development, and writing; You Sung Seo: study concept and design, acquisition and analysis of data, and manuscript authorization.

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Correspondence to You Sung Seo.

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Jang, S.H., Seo, Y.S. Title: Injury characteristics of the Papez circuit in patients with diffuse axonal injury: a diffusion tensor tractography study. Acta Neurol Belg 121, 941–947 (2021). https://doi.org/10.1007/s13760-020-01485-1

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  • DOI: https://doi.org/10.1007/s13760-020-01485-1

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