Advertisement

Neuroradiological and clinical features in ophthalmoplegia

  • Stefan WeidauerEmail author
  • Christian Hofmann
  • Marlies Wagner
  • Elke Hattingen
Review

Abstract

Purpose

Especially in acute onset of ophthalmoplegia, efficient neuroradiological evaluation is necessary to assist differential diagnosis, clinical course, and treatment options.

Methods

Different manifestations of ophthalmoplegia are explained and illustrated by characteristic neuroradiological and clinical findings.

Results

To present those ophthalmoplegic disorders in a clear manner, this review refers to different neuroanatomical structures and compartments. From neuroophthalmological point of view, diseases going ahead with ophthalmoplegia can be divided into (1) efferent infranuclear/peripheral disturbances involving oculomotor cranial nerves, (2) conjugate gaze abnormalities due to internuclear or supranuclear lesions, and (3) diseases of the extraocular eye muscles or their impairment due to intraorbital pathologies.

Conclusion

The knowledge of the relationship between neurological findings in ophthalmoplegia and involved neuroanatomical structures is crucial, and neuroradiology can be focused on circumscribed anatomical regions, using optimized investigation protocols.

Keywords

Ophthalmoplegia MRI Cranial nerve palsy Conjugate gaze abnormality Horner syndrome 

Notes

Acknowledgments

We thank Dr. Michael Nichtweiß for generously offering his advice and expertise during the process of this review.

Funding

No funding was received for this study.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in the studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual participants included in the study.

References

  1. 1.
    Liu GT, Volpe NJ, Galetta ST Neuro-Ophthalmology: Diagnosis and Management, 3rd edn. Elsevier, EdinburghGoogle Scholar
  2. 2.
    Danieli L, Montali M, Remonda L et al (2018) Clinically directed neuroimaging of ophthalmoplegia. Clin Neuroradiol 28:3–16CrossRefPubMedGoogle Scholar
  3. 3.
    Strupp M, Kremmyda O, Adamczyk C et al (2014) Central ocular motor disorders, including gaze palsy and nystagmus. J Neurol 261(Suppl 2):S542–S558CrossRefPubMedGoogle Scholar
  4. 4.
    Strupp M, Hüfner K, Sandmann R, Zwergal A, Dieterich M, Jahn K, Brandt T (2011) Central oculomotor disturbances and nystagmus—a window into the brainstem and cerebellum. Dtsch Arztebl Int 108:197–204PubMedPubMedCentralGoogle Scholar
  5. 5.
    Bähr M, Frotscher M (2012) Duus' topical diagnosis in neurology: anatomy, physiology, signs, symptoms, 5th edn. Georg Thieme Verlag, StuttgartGoogle Scholar
  6. 6.
    Meyer A (1920) Herniation of the brain. Arch Neurol Psychiatr 4:387–400CrossRefGoogle Scholar
  7. 7.
    Berlit P (1991) Isolated and combined pareses of cranial nerves III, IV and VI. A retrospective study of 412 patients. J Neurol Sci 103:10–15CrossRefPubMedGoogle Scholar
  8. 8.
    Adams ME, Linn J, Yousry I (2008) Pathology of the ocular motor nerves III, IV, and VI. Neuroimaging Clin N Am 18:261–282CrossRefPubMedGoogle Scholar
  9. 9.
    Weber A, Romo LV, Sabates NR (1999) Pseudotumor of the orbit. Clinical, pathologic, and radiologic evaluation. Radiol Clin N Am 37:151–168CrossRefPubMedGoogle Scholar
  10. 10.
    Sahlmüller M, Schroeter J (2011) Idiopathic inflammatory orbitopathy. Augenheilkunde up2date 1:15–30CrossRefGoogle Scholar
  11. 11.
    Kashii S (2014) IgG4-related disease: a neuro-ophthalmological perspective. J Neuroophthalmol 34:400–407CrossRefPubMedGoogle Scholar
  12. 12.
    Purohit BS, Vargas MI, Ailiano A, Merlini L, Poletti PA, Platon A, Delattre BM et al (2016) Orbital tumours and tumour-like lesions: exploring the armamentarium of multiparametric imaging. Insights Imaging 7:43–68CrossRefPubMedGoogle Scholar
  13. 13.
    van der Pol CB, Chakraborty S, Gao J, Nguyen T, Torres C, Glikstein R (2014) Imaging anatomy and pathology of extraocular muscles in adults. Can Assoc Radiol J 65:366–371CrossRefPubMedGoogle Scholar
  14. 14.
    Blitz AM, Macedo LL, Chonka ZD, Ilica AT, Choudhri AF, Gallia GL, Aygun N (2014) High-resolution CISS MR imaging with and without contrast for evaluation of the upper cranial nerves: segmental anatomy and selected pathologic conditions of the cisternal through extraforaminal segments. Neuroimaging Clin N Am 24:17–34CrossRefPubMedGoogle Scholar
  15. 15.
    Yousry I, Camelio S, Schmid UD, Horsfield MA, Wiesmann M, Brückmann H, Yousry TA (2000) Visualization of cranial nerves I-XII: value of 3D CISS and T2-weighted FSE sequences. Eur Radiol 10:1061–1067CrossRefPubMedGoogle Scholar
  16. 16.
    Wen J, Desai NS, Jeffery D, Aygun N, Blitz A (2018) High-resolution isotropic three-dimensional MR imaging of the extraforaminal segments of the cranial nerves. Magn Reson Imaging Clin N Am 26:101–119CrossRefPubMedGoogle Scholar
  17. 17.
    Yousry I, Camelio S, Wiesmann M, Schmid UD, Moriggl B, Brückmann H, Yousry TA (1999) Detailed magnetic resonance imaging anatomy of the cisternal segment of the abducent nerve: Dorello's canal and neurovascular relationships and landmarks. J Neurosurg 91:276–283CrossRefPubMedGoogle Scholar
  18. 18.
    Villain M, Segnarbieux F, Bonnel F, Aubry I, Arnaud B (1993) The trochlear nerve: anatomy by microdissection. Surg Radiol Anat 15:169–173CrossRefPubMedGoogle Scholar
  19. 19.
    Hattingen E, Blasel S, Nichtweiss M, Zanella FE, Weidauer S (2010) MR imaging of midbrain pathologies. Clin Neuroradiol 20:81–97CrossRefPubMedGoogle Scholar
  20. 20.
    Thömke F (2004) Brainstem diseases causing isolated ocular motor nerve palsies. Neuro-Ophthalmology 28:53–67CrossRefGoogle Scholar
  21. 21.
    Kücker W, Weise J, Krapf H, Schmidt F, Friese S, Bähr M (2002) MRI characteristics of acute and subacute brainstem and thalamic infarctions: value of T2- and diffusion-weighted sequences. J Neurol 249:33–42CrossRefGoogle Scholar
  22. 22.
    Linn J, Peters F, Lummel N, Schankin C, Rachinger W, Brueckmann H, Yousry I (2011) Detailed imaging of the normal anatomy and pathologic conditions of the cavernous region at 3 Tesla using a contrast-enhanced MR angiography. Neuroradiology 53:947–954CrossRefPubMedGoogle Scholar
  23. 23.
    Castaigne P, Lhermitte F, Buge A, Escourolle R, Hauw JJ, Lyon-Caen O (1981) Paramedian thalamic and midbrain infarcts: clinical and neuropathological study. Ann Neurol 10:127–148CrossRefPubMedGoogle Scholar
  24. 24.
    Schlesinger B (1976) The upper brainstem in the human. Its nuclear configuration and vascular supply. Springer, Berlin, pp 46–139CrossRefGoogle Scholar
  25. 25.
    Weidauer S, Moreitz S, Nichtweiss M (2018) Painful oculomotor nerve palsy. Dtsch Arztebl Int 115:298PubMedPubMedCentralGoogle Scholar
  26. 26.
    Güresir E, Schuss P, Seifert V, Vatter H (2012) Oculomotor nerve palsy by posterior communicating artery aneurysms: influence of surgical strategy on recovery. J Neurosurg 117:904–910CrossRefPubMedGoogle Scholar
  27. 27.
    Gabarel T, Borha A, di Palma C et al (2016) Clipping versus coiling in the management of posterior communicating artery aneurysms with third nerve palsy: a systematic review and meta-analysis. World Neurosurg 87:498–5067CrossRefGoogle Scholar
  28. 28.
    Panagiotopoulos V, Ladd SC, Gizewski E, Asgari S, Sandalcioglu EI, Forsting M, Wanke I (2011) Recovery of ophthalmoplegia after endovascular treatment of intracranial aneurysms. AJNR Am J Neuroradiol 32:276–282CrossRefPubMedGoogle Scholar
  29. 29.
    Fu Q, Guan S, Liu C, Wang K, Cheng J (2018) Clinical significance of circumferential aneurysmal wall enhancement in symptomatic patients with unruptured intracranial aneurysms: a high-resolution MRI study. Clin Neuroradiol 28:509–514CrossRefPubMedGoogle Scholar
  30. 30.
    Fujiwara S, Fujii K, Nishio S, Matsushima T, Fukui M (1989) Oculomotor nerve palsy in patients with cerebral aneurysms. Neurosurg Rev 12:123–132CrossRefPubMedGoogle Scholar
  31. 31.
    Gagliardi D, Faravelli I, Villa L, Pero G, Cinnante C, Brusa R et al (2018) Bilateral cavernous carotid aneurysms: atypical presentation of a rare cause of mass effect. A case report and a review of the literature. Front Neurol 9:619CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Duane A (1996) Congenital deficiency of abduction, associated with impairment of adduction, retraction movements, contraction of the palpebral fissure and oblique movements of the eye. Arch Ophthalmol 1905;34:133–159Google Scholar
  33. 33.
    Huber A (1974) Electrophysiology of the retraction syndromes. Br J Ophthalmol 58:293–300CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Kekunnaya R, Negalur M (2017) Duane retraction syndrome: causes, effects and management strategies. Clin Ophthalmol 11:1917–1930CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Xia S, Li RL, Li YP et al (2014) MRI findings in Duane’s ocular retraction syndrome. Clin Radiol 69e:191–198CrossRefGoogle Scholar
  36. 36.
    Kim JH, Hwang JM (2017) Imaging of cranial nerves III, IV, VI in congenital cranial dysinnervation disorders. Korean J Ophthalmol 31:183–193CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Tuzcu EA, Bayarogullari H, Atci N, Basarslan F, Coskun M, Yilmaz C, Ilhan N, Daglioglu M (2014) Magnetic resonance imaging findings of the abducens nerves in type 1 Duane's retraction syndrome. Semin Ophthalmol 29:142–145CrossRefPubMedGoogle Scholar
  38. 38.
    Schievink WI (2006) Spontaneous spinal cerebrospinal fluid leaks and intracranial hypotension. JAMA 295:2286–2296CrossRefPubMedGoogle Scholar
  39. 39.
    Zada G, Solomon TC, Giannotta SL (2007) A review of ocular manifestations in intracranial hypotension. Neurosurg Focus 23:E8CrossRefPubMedGoogle Scholar
  40. 40.
    Moster SJ, Moster ML (2014) Alternating skew deviation from traumatic intracranial hypotension. Neuro-Ophthalmology 38:156–158CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Vahdani K, McVeigh K, Harrison R, Williams M, Garrott H (2018) Intracranial hypotension mimicking chronic progressive external ophthalmoplegia. Orbit 37:371–374CrossRefPubMedGoogle Scholar
  42. 42.
    Dandurand C, Haw CS (2016) Oculomotor palsy in spontaneous intracranial hypotension: case report and review of the literature. Can J Neurol Sci 43:747–749CrossRefPubMedGoogle Scholar
  43. 43.
    Ono K, Arai H, Endo T, Tsunoda A, Sato K, Sakai T, Makita J (2004) Detailed MR imaging anatomy of the abducens nerve: evagination of CSF into Dorello canal. AJNR Am J Neuroradiol 25:623–626PubMedGoogle Scholar
  44. 44.
    Icke C, Ozer E, Arda N (2010) Microanatomical characteristics of the petrosphenoidal ligament of Gruber. Turk Neurosurg 20:323–327PubMedGoogle Scholar
  45. 45.
    Kanagalingam S, Miller N (2015) Horner syndrome: clinical perspectives. Eye Brain 7:35–46PubMedPubMedCentralGoogle Scholar
  46. 46.
    Striph GG, Burde RM (1988) Abducens nerve palsy and Horner’s syndrome revisited. J Clin Neuroophthalmol 8:13–17PubMedGoogle Scholar
  47. 47.
    Tolosa E (1954) Periarteritic lesions of the carotid siphon with clinical features of a carotid infraclinoid aneurysm. J Neurol Neurosurg Psychiatry 17:300–302CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Hunt WE, Meagher JN, LeFever HE et al (1961) Painful ophthalmoplegia: its relation to indolent inflammation of the cavernous sinus. Neurology 11:56–62CrossRefPubMedGoogle Scholar
  49. 49.
    Kline LB, Hoyt WF (2001) The Tolosa-Hunt syndrome. J Neurol Neurosurg Psychiatry 71:577–582CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Headache Classification Committee of the International Headache Society (IHS) (2018) The international classification of headache disorders, 3rd edition. Cephalalgia 38:1–211Google Scholar
  51. 51.
    Schuknecht B, Sturm V, Huismana TAGM et al (2009) Tolosa-Hunt syndrome: MR imaging features in 15 patients with 20 episodes of painful ophthalmoplegia. Eur J Radiol 69:445–453CrossRefPubMedGoogle Scholar
  52. 52.
    Wasmeier C, Pfadenhauer K, Rößler A (2002) Idiopathic inflammatory pseudotumor of the orbit and Tolosa-Hunt syndrome—are they the same disease? J Neurol 249:1237–1241CrossRefPubMedGoogle Scholar
  53. 53.
    Yamamoto M, Hashimoto M, Takahashi H, Shinomura Y (2014) IgG4 disease. J Neuroophthalmol 34:393–399CrossRefPubMedGoogle Scholar
  54. 54.
    Stone HJ, Zen Y, Deshpande V (2012) IgG4-related disease. N Engl J Med 366:539–551CrossRefGoogle Scholar
  55. 55.
    Wallace ZS, Deshpande V, Stone JH (2014) Ophthalmic manifestations of IgG4-related disease: single-center experience and literature review. Semin Arthritis Rheum 43:806–817CrossRefPubMedGoogle Scholar
  56. 56.
    Wong AJ, Planck SR, Choi D, Harrington CA, Troxell ML, Houghton DC, Stauffer P, Wilson DJ, Grossniklaus HE, Dailey RA, Ng JD, Steele EA, Harris GJ, Czyz C, Foster JA, White VA, Dolman PJ, Kazim M, Patel PJ, Edward DP, Katan H, Hussain H, Selva D, Yeatts RP, Korn BS, Kikkawa DO, Rosenbaum JT (2014) IgG4 immunostaining and its implications in orbital inflammatory disease. PLoS One 9:e109847CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Andrew N, Kearney D, Selva D (2013) IgG4-related orbital disease: a meta-analysis and review. Acta Ophthalmol 91:694–700CrossRefPubMedGoogle Scholar
  58. 58.
    Bosch J, Ortega-Aznar A, Tintore M et al (2000) Hypertrophic pachymeningitis. A review of the histories of two cases and pathological relationship with the Tolosa-Hunt syndrome and the orbital pseudotumor. Rev Neurol 31:946–951PubMedGoogle Scholar
  59. 59.
    Boban J, Ardalı S, Thurnher MM (2018) Leptomeningeal form of immunoglobulin G4-related hypertrophic meningitis with perivascular spread: a case report and review of the literature. Neuroradiology 60:769–773CrossRefPubMedCentralGoogle Scholar
  60. 60.
    Barrow DL, Spector RH, Braun IF, Landman JA, Tindall SC, Tindall GT (1985) cClassification and treatment of spontaneous carotid-cavernous sinus fistulas. J Neurosurg 62:248–256CrossRefPubMedGoogle Scholar
  61. 61.
    Ringer AJ, Salud L, Tomsick TA (2005) Carotid cavernous fistulas: anatomy, classification, and treatment. Neurosurg Clin N Am 16:279–295CrossRefPubMedGoogle Scholar
  62. 62.
    Henderson AD, Miller NR (2018) Carotid-cavernous fistula: current concepts in aetiology, investigation, and management. Eye 32:164–172CrossRefPubMedGoogle Scholar
  63. 63.
    de Keizer R (2003) Carotid-cavernous and orbital arteriovenous fistulas: ocular features, diagnostic and hemodynamic considerations in relation to visual impairment and morbidity. Orbit 22:121–142CrossRefPubMedGoogle Scholar
  64. 64.
    Coskun O, Hamon M, Catroux G, Gosme L, Courtheoux P, Theron J (2000) Carotid-cavernous fistulas: diagnosis with spiral CT angiography. AJNR Am J Neuroradiol 21:712–716PubMedGoogle Scholar
  65. 65.
    Hirai T, Korogi Y, Hamatake S, Ikushima I, Sugahara T, Sigematsu Y, Higashida Y, Takahashi M (1998) Three-dimensional FISP imaging in the evaluation of carotid cavernous fistula: comparison with contrast-enhanced CT and spin-echo MR. AJNR Am J Neuroradiol 19:253–259PubMedGoogle Scholar
  66. 66.
    Seeger A, Kramer U, Bischof F, Schuettauf F, Ebner F, Danz S, Ernemann U, Hauser TK (2015) Feasibility of noninvasive diagnosis and treatment planning in a case series with carotid-cavernous fistula using high-resolution time-resolved MR-angiography with stochastic trajectories (TWIST) and extended parallel acquisition technique (ePAT 6) at 3 T. Clin Neuroradiol 25:241–247CrossRefPubMedGoogle Scholar
  67. 67.
    Gemmete J, Chaudhary N, Pandey A et al (2010) Treatment of carotid cavernous fistulas. Curr Treat Options Neurol 12:43–53CrossRefPubMedGoogle Scholar
  68. 68.
    Fisher M (1956) An unusual variant of acute idiopathic polyneuritis (syndrome of ophthalmoplegia, ataxia and areflexia). N Engl J Med 255:57–65CrossRefPubMedGoogle Scholar
  69. 69.
    Bickerstaff ER, Cloake PC (1951) Mesencephalitis and Rhomencephalitis. Br Med J 2:77–81CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Shahrizaila N, Yuki N (2013) Bickerstaff brainstem encephalitis and Fisher syndrome: anti-GQ1b antibody syndrome. J Neurol Neurosurg Psychiatry 84:576–583CrossRefPubMedGoogle Scholar
  71. 71.
    Ito M, Kuwabara S, Odaka M, Misawa S, Koga M, Hirata K, Yuki N (2008) Bickerstaff’s brainstem encephalitis and Fisher syndrome form a continuous spectrum. Clinical analysis of 581 cases. J Neurol 255:674–682CrossRefPubMedGoogle Scholar
  72. 72.
    Gologorsky RC, Barakos JA, Sahebkar F (2013) Rhomb- and Bickerstaff encephalitis: two clinical phenotypes? Pediatr Neurol 48:244–248CrossRefPubMedGoogle Scholar
  73. 73.
    Santoro JD, Lazzareschi DV, Campen CJ, Van Haren KP (2018) Pediatric Bickerstaff brainstem encephalitis: a systematic review of literature and case series. J Neurol 265:141–150CrossRefPubMedGoogle Scholar
  74. 74.
    Odaka M, Yuki N, Yamada M, Koga M, Takemi T, Hirata K, Kuwabara S (2003) Bickerstaff's brainstem encephalitis: clinical features of 62 cases and a subgroup associated with Guillain-Barré syndrome. Brain 126:2279–2290CrossRefPubMedGoogle Scholar
  75. 75.
    Wakerley BR, Uncini A, Yuki N GBS Classification Group (2014) Guillain-Barré and Miller Fisher syndromes—new diagnostic classification. Nat Rev Neurol 10:537–544 Erratum in: Nat Rev Neurol 2014;10:612Google Scholar
  76. 76.
    Drier A, Haroche J, Savatovsky J, Godenèche G, Dormont D, Chiras J, Amoura Z, Bonneville F (2010) Cerebral, facial, and orbital involvement in Erdheim-Chester disease: CT and MR imaging findings. Radiology 255:586–594CrossRefPubMedGoogle Scholar
  77. 77.
    Weidauer S, von Stuckrad-Barre S, Dettmann E, Zanella FE, Lanfermann H (2003) Cerebral Erdheim-Chester disease: case report and review of the literature. Neuroradiology 45:241–245CrossRefPubMedGoogle Scholar
  78. 78.
    Lachenal F, Cotton F, Desmurs-Clavel H, Haroche J, Taillia H, Magy N, Hamidou M, Salvatierra J, Piette JC, Vital-Durand D, Rousset H (2006) Neurological manifestations and neuroradiological presentation of Erdheim-Chester disease: report of 6 cases and systematic review of the literature. J Neurol 253:1267–1277CrossRefPubMedGoogle Scholar
  79. 79.
    Wright RA, Hermann RC, Parisi JE (1999) Neurological manifestations of Erdheim-Chester disease. J Neurol Neurosurg Psychiatry 66:72–75CrossRefPubMedPubMedCentralGoogle Scholar
  80. 80.
    Caparros-Lefebvre D, Pruvo JP, Rémy M, Wallaert B, Petit H (1995) Neuroradiologic aspects of Erdheim-Chester disease. AJNR Am J Neuroradiol 16:735–740PubMedGoogle Scholar
  81. 81.
    Martinez R (1995) Erdheim-Chester disease: MR of intraaxial and extraaxial brain stem lesions. AJNR Am J Neuroradiol 16:1787–1790PubMedGoogle Scholar
  82. 82.
    Evidente VG, Adler CH, Giannini C, Conley CR, Parisi JE, Fletcher GP (1998) Erdheim-Cheser disease with extensive intraaxial brain stem lesions presenting as a progressive cerebellar syndrome. Mov Disord 13:576–581CrossRefPubMedGoogle Scholar
  83. 83.
    Berkman J, Ford C, Johnson E, Malow BA, Aulino JM (2018) Misdiagnosis: CNS Erdheim-Chester disease mimicking CLIPPERS. Neuroradiol J 31:399–402CrossRefPubMedGoogle Scholar
  84. 84.
    Al Bayati A, Plate T, Al Bayati M, Yan Y, Lavi ES, Rosenblatt JD (2018) Dabrafenib and Trametinib treatment for Erdheim-Chester disease with brain stem involvement. Mayo Clin Proc Innov Qual Outcomes 4:303–308CrossRefGoogle Scholar
  85. 85.
    Frohman EM, Zhang H, Kramer PD, Fleckenstein J, Hawker K, Racke MK, Frohman TC (2001) MRI characteristics of the MLF in MS patients with chronic internuclear ophthalmoparesis. Neurology 57:762–768CrossRefPubMedGoogle Scholar
  86. 86.
    Wattjes MP, Steenwijk MD, Stangel M (2015) MRI in the diagnosis and monitoring of multiple sclerosis: an update. Clin Neuroradiol 25(Suppl 2):157–165CrossRefPubMedGoogle Scholar
  87. 87.
    Traboulsee A, Simon JH, Stone L, Fisher E, Jones DE, Malhotra A, Newsome SD, Oh J, Reich DS, Richert N, Rammohan K, Khan O, Radue EW, Ford C, Halper J, Li D (2016) Revised recommendations of the consortium of MS centers task force for a standardized MRI protocol and clinical guidelines for the diagnosis and follow-up of multiple sclerosis. AJNR Am J Neuroradiol 37:394–401CrossRefPubMedGoogle Scholar
  88. 88.
    Filippi M, Rocca M, Ciccarelli O, de Stefano N, Evangelou N, Kappos L, Rovira A, Sastre-Garriga J, Tintorè M, Frederiksen JL, Gasperini C, Palace J, Reich DS, Banwell B, Montalban X, Barkhof F, MAGNIMS Study Group (2016) MRI criteria for the diagnosis of multiple sclerosis: MAGNIMS consensus guidelines. Lancet Neurol 15:292–303CrossRefPubMedPubMedCentralGoogle Scholar
  89. 89.
    Wattjes MP, Raab P (2018) Brain and spinal cord MRI in multiple sclerosis: an update. Akt Neurol 45:29–43CrossRefGoogle Scholar
  90. 90.
    Duvernoy H (1978) Human brainstem vessels. Springer, BerlinCrossRefGoogle Scholar
  91. 91.
    Tatu L, Moulin T, Bogousslavsky J, Duvernoy H (1996) Arterial territories of human brain: brainstem and cerebellum. Neurology 47:1125–1135CrossRefPubMedGoogle Scholar
  92. 92.
    Kim JS (2004) Internuclear ophthalmoplegia as an isolated or predominant symptom of brainstem infarction. Neurology 62:1491–1496CrossRefPubMedGoogle Scholar
  93. 93.
    Pierrot-Deseilligny C, Chain F, Serdaru M et al (1981) The ‘one-and-a-half’ syndrome. Electro-oculographic analyses of five cases with deductions about the physiological mechanisms of lateral gaze. Brain 104:669–699CrossRefGoogle Scholar
  94. 94.
    Deleu D, Solheid C, Michotte A, Ebinger G (1988) Dissociated ipsilateral horizontal gaze palsy in one-and-a-half syndrome. Neurology 38:1278–1280CrossRefPubMedGoogle Scholar
  95. 95.
    Eggenberger E (1998) Eight-and-a-half syndrome: one-and-a-half syndrome plus cranial nerve VII palsy. J Neuroophthalmol 18:114–116PubMedGoogle Scholar
  96. 96.
    Skaat A, Huna-Baron R (2012) Eight-and-a-half syndrome: a rare pontine neuroophthalmic syndrome. Arch Neurol 69:934–935CrossRefPubMedGoogle Scholar
  97. 97.
    Uysal S, Demirtas-Tatlidede A, Selcuk OY, Yayla V (2013) Diffusion-weighted imaging in eight-and-a-half syndrome presenting with transient hemiparesis. Clin Neuroradiol 23:235–236CrossRefPubMedGoogle Scholar
  98. 98.
    Victor M, Adams RD, Collins GH (1971) The Wernicke–Korsakoff syndrome: a clinical and pathological study of 245 patients, 82 with post-mortem examinations. Contemp Neurol Ser 7:1–206PubMedGoogle Scholar
  99. 99.
    Weidauer S, Nichtweiss M, Lanfermann H, Zanella FE (2003) Wernicke encephalopathy: MR findings and clinical presentation. Eur Radiol 13:1001–1009PubMedGoogle Scholar
  100. 100.
    Antunez E, Estruch R, Cardenal C, Nicolas JM, Fernandez-Sola J, Urbano-Marquez A (1998) Usefulness of CT and MR imaging in the diagnosis of acute Wernicke’s encephalopathy. AJR Am J Roentgenol 171:1131–1137CrossRefPubMedGoogle Scholar
  101. 101.
    Suzuki S, Ichijo M, Fujii H, Matsuoka Y, Ogawa Y (1996) Acute Wernicke’s encephalopathy: comparison of magnetic resonance images and autopsy findings. Intern Med 35:831–834CrossRefPubMedGoogle Scholar
  102. 102.
    Zuccoli G, Santa Cruz D, Bertolini M, Rovira A, Gallucci M, Carollo C, Pipitone N (2009) MR imaging findings in 56 patients with Wernicke encephalopathy: nonalcoholics may differ from alcoholics. AJNR Am J Neuroradiol 30:171–176CrossRefPubMedGoogle Scholar
  103. 103.
    Weidauer S, Rösler A, Zanella FE, Lanfermann H (2004) Diffusion-weighted imaging in Wernicke encephalopathy associated with stomach cancer: case report and review of the literature. Eur Neurol 51:55–57CrossRefPubMedGoogle Scholar
  104. 104.
    White ML, Zhang Y, Andrew LG, Hadley WL (2005) MR imaging with diffusion-weighted imaging in acute and chronic Wernicke encephalopathy. AJNR Am J Neuroradiol 26:2306–2310PubMedGoogle Scholar
  105. 105.
    Weidauer S, Ziemann U, Thomalske C, Gaa J, Lanfermann H, Zanella FE (2003) Vasogenic edema in Bickerstaff’s brainstem encephalitis. A serial MRI study. Neurology 61:836–838CrossRefPubMedGoogle Scholar
  106. 106.
    Kearns T, Sayre G (1958) Retinitis pigmentosa, external ophthalmoplegia, and complete heart block. Arch Ophthalmol 60:280–289CrossRefGoogle Scholar
  107. 107.
    Graff-Radford NR, Eslinger PJ, Damasio AR (1984) Nonhemorrhagic infarction of the thalamus: behavioral, anatomic, and physiologic correlates. Neurology 34:14–23CrossRefPubMedGoogle Scholar
  108. 108.
    Segarra JM (1970) Cerebral vascular disease and behaviour. The syndrome of the mesencephalic artery. Arch Neurol 22:408–418CrossRefPubMedGoogle Scholar
  109. 109.
    Bogousslavsky J, Regli F, Uske A (1988) Thalamic infarcts: clinical syndromes, etiology and prognosis. Neurology 38:837–848 Erratum 1988;38:1335CrossRefPubMedGoogle Scholar
  110. 110.
    Caplan LR (1980) “Top of the basilar” syndrome. Neurology 30:72–79CrossRefPubMedGoogle Scholar
  111. 111.
    Weidauer S, Nichtweiß M, Zanella FE, Lanfermann H (2004) Assessment of paramedian thalamic infarcts: MR imaging, clinical features and prognosis. Eur Radiol 14:1615–1626CrossRefPubMedGoogle Scholar
  112. 112.
    Bender MB (1980) Brain control of conjugate horizontal and vertical eye movements. A survey of the structural and functional correlates. Brain 103:23–69CrossRefPubMedGoogle Scholar
  113. 113.
    Percheron G (1976) Arteries of the human thalamus. I Artery and polar thalamic territory of the posterior communicating artery. Rev Neurol (Paris) 132:297–307Google Scholar
  114. 114.
    Percheron G (1976) Arteries of the human thalamus. II. Arteries and paramedian thalamic territory of the communicating basilar artery. Rev Neurol (Paris) 132:309–324Google Scholar
  115. 115.
    Lazorthes G, Salamon G (1971) The arteries of the thalamus. J Neurosurg 34:23–26CrossRefPubMedGoogle Scholar
  116. 116.
    Marinkovic SV, Milisavljevic MM, Kovacevic MS (1986) Anastomoses among the thalamoperforating branches of the posterior cerebral artery. Arch Neurol 43:811–814CrossRefPubMedGoogle Scholar
  117. 117.
    Schmahmann JD (2003) Vascular syndromes of the thalamus. Stroke 34:2264–2278CrossRefPubMedGoogle Scholar
  118. 118.
    Deleu D (1997) Selective vertical saccadic palsy from unilateral medial thalamic infarction: clinical, neurophysiologic and MRI correlates. Acta Neurol Scand 96:332–336CrossRefPubMedGoogle Scholar
  119. 119.
    Wiest G, Baumgartner C, Schnider P, Trattnig S, Deecke L, Mueller C (1996) Monocular elevation paresis and contralateral downgaze paresis from unilateral mesodiencephalic infarction. J Neurol Neurosurg Psychiatry 60:579–581CrossRefPubMedPubMedCentralGoogle Scholar
  120. 120.
    Clark JM, Albers GW (1995) Vertical gaze palsies from medial thalamic infarctions without midbrain involvement. Stroke 26:1467–1470CrossRefPubMedGoogle Scholar
  121. 121.
    Steele JC, Richardson JC, Olszewski J (1964) Progressive supranuclear palsy: a heterogeneous degeneration involving the brainstem, basal ganglia and cerebellum with vertical supranuclear gaze and pseudobulbar palsy, nuchal dystonia and dementia. Arch Neurol 10:333–359CrossRefPubMedGoogle Scholar
  122. 122.
    Respondek G, Levin J, Höglinger GU (2018) Progressive supranuclear palsy and multiple system atrophy: clinicopathological concepts and therapeutic challenges. Curr Opin Neurol 31:448–454PubMedGoogle Scholar
  123. 123.
    Höglinger GU, Respondek G, Stamelou M, Kurz C, Josephs KA, Lang AE, Mollenhauer B, Müller U, Nilsson C, Whitwell JL, Arzberger T, Englund E, Gelpi E, Giese A, Irwin DJ, Meissner WG, Pantelyat A, Rajput A, van Swieten JC, Troakes C, Antonini A, Bhatia KP, Bordelon Y, Compta Y, Corvol JC, Colosimo C, Dickson DW, Dodel R, Ferguson L, Grossman M, Kassubek J, Krismer F, Levin J, Lorenzl S, Morris HR, Nestor P, Oertel WH, Poewe W, Rabinovici G, Rowe JB, Schellenberg GD, Seppi K, van Eimeren T, Wenning GK, Boxer AL, Golbe LI, Litvan I, for the Movement Disorder Society-endorsed PSP Study Group (2017) Clinical diagnosis of progressive supranuclear palsy: the movement disorder society criteria. Mov Disord 32:853–864CrossRefPubMedPubMedCentralGoogle Scholar
  124. 124.
    Whitwell JL, Höglinger GU, Antonini A, Bordelon Y, Boxer AL, Colosimo C, van Eimeren T, Golbe LI, Kassubek J, Kurz C, Litvan I, Pantelyat A, Rabinovici G, Respondek G, Rominger A, Rowe JB, Stamelou M, Josephs KA, for the Movement Disorder Society-endorsed PSP Study Group (2017) Radiological biomarkers for diagnosis in PSP: where are we and where do we need to be? Mov Disord 32:955–971CrossRefPubMedPubMedCentralGoogle Scholar
  125. 125.
    Warmuth-Metz M, Naumann M, Csoti I, Solymosi L (2001) Measurement of the midbrain diameter on routine magnetic resonance imaging: a simple and accurate method of differentiating between Parkinson disease and progressive supranuclear palsy. Arch Neurol 58:1076–1079CrossRefPubMedGoogle Scholar
  126. 126.
    Adachi M, Kawanami T, Ohshima H et al (2004) Morning glory sign: a particular MR finding in progressive supranuclear palsy. Magn Reson Med Sci 3:125–132CrossRefPubMedGoogle Scholar
  127. 127.
    Möller L, Kassubek J, Südmeyer M, Hilker R, Hattingen E, Egger K, Amtage F, Pinkhardt EH, Respondek G, Stamelou M, Möller F, Schnitzler A, Oertel WH, Knake S, Huppertz HJ, Höglinger GU (2017) Manual MRI morphometry in parkinsonian syndromes. Mov Disord 32:778–782CrossRefPubMedGoogle Scholar
  128. 128.
    Doraiswamy PM, Na C, Husain MM, Figiel GS, McDonald W, Ellinwood EH Jr, Boyko OB, Krishnan KR (1992) Morphometric changes of the human midbrain with normal aging: MR and stereologic findings. AJNR Am J Neuroradiol 13:383–386PubMedGoogle Scholar
  129. 129.
    Huppertz HJ, Moller L, Sudmeyer M et al (2016) Differentiation of neurodegenerative parkinsonian syndromes by volumetric magnetic resonance imaging analysis and support vector machine classification. Mov Disord 31:1506–1517CrossRefPubMedGoogle Scholar
  130. 130.
    Lapras C, Bognar L, Turjman F, Villanyi E, Mottolese C, Fischer C et al (1994) Tectal plate gliomas. Part I: Microsurgery of the tectal plate gliomas. Acta Neurochir (Wien) 126:76–83CrossRefGoogle Scholar
  131. 131.
    Ternier J, Wray A, Puget S, Bodaert N, Zerah M, Sainte-Rose C (2006) Tectal plate lesions in children. J Neurosurg 104:369–376PubMedGoogle Scholar
  132. 132.
    Ferreira TA, Saraiva P, Genders SW, Buchem MV, Luyten GPM, Beenakker JW (2018) CT and MR imaging of orbital inflammation. Neuroradiology 60:1253–1266CrossRefPubMedPubMedCentralGoogle Scholar
  133. 133.
    Bhatti MT (2007) Orbital syndromes. Semin Neurol 27:269–287CrossRefPubMedGoogle Scholar
  134. 134.
    Schoser BG (2007) Ocular myositis: diagnostic assessment, differential diagnoses, and therapy of a rare muscle disease—five new cases and review. Clin Ophthalmol 1:37–42PubMedPubMedCentralGoogle Scholar
  135. 135.
    Lacey B, Chang W, Rootman J (1999) Nonthyroid causes of extraocular muscle disease. Surv Ophthalmol 44:187–213CrossRefPubMedGoogle Scholar
  136. 136.
    Montagnese F, Wenninger S, Schoser B (2016) "Orbiting around" the orbital myositis: clinical features, differential diagnosis and therapy. J Neurol 263:631–640CrossRefPubMedGoogle Scholar
  137. 137.
    Fischer M, Kempkes U, Haage P, Isenmann S (2010) Recurrent orbital myositis mimicking sixth nerve palsy: diagnosis with MR imaging. AJNR Am J Neuroradiol 31:275–276CrossRefPubMedGoogle Scholar
  138. 138.
    Garau LM, Guerrieri D, De Cristofaro F, Bruscolini A, Panzironi G (2018) Extraocular muscle sampled volume in Graves’ orbitopathy using 3-T fast spin-echo MRI with iterative decomposition of water and fat sequences. Acta Radiol Open 7:2058460118780892PubMedPubMedCentralGoogle Scholar
  139. 139.
    Politi LS, Godi C, Cammarata G, Ambrosi A, Iadanza A, Lanzi R, Falini A, Bianchi Marzoli S (2014) Magnetic resonance imaging with diffusion-weighted imaging in the evaluation of thyroid-associated orbitopathy: getting below the tip of the iceberg. Eur Radiol 24:1118–1126CrossRefPubMedGoogle Scholar
  140. 140.
    Lingam RK, Mundada P, Lee V (2018) Novel use of non-echo-planar diffusion weighted MRI in monitoring disease activity and treatment response in active Grave's orbitopathy: an initial observational cohort study. Orbit 10:1–6Google Scholar
  141. 141.
    Daubner D, Spieth S, Engellandt K, von Kummer R (2012) Diagnosis and differential diagnosis of Graves' orbitopathy in MRI. Radiologe 52:550–559CrossRefPubMedGoogle Scholar
  142. 142.
    Gerlach M, Ferbert A (2008) Pure eye muscle involvement in endocrine orbitopathy. Eur Neurol 60:67–72CrossRefPubMedGoogle Scholar
  143. 143.
    Schoser BG, Pongratz D (2006) Extraocular mitochondrial myopathies and their differential diagnoses. Strabismus 14:107–113CrossRefPubMedGoogle Scholar
  144. 144.
    Mombaerts I, Bilyk JR, Rose GE, McNab AA, Fay A, Dolman PJ et al (2017) Consensus on diagnostic criteria of idiopathic orbital inflammation using a modified Delphi approach. JAMA Ophthalmol 135:769–776CrossRefPubMedPubMedCentralGoogle Scholar
  145. 145.
    Yeşiltaş YS, Gündüz AK (2018) Idiopathic orbital inflammation: review of literature and new advances. Middle East Afr J Ophthalmol 25:71–80CrossRefPubMedPubMedCentralGoogle Scholar
  146. 146.
    Beebe JD, Kardon RH, Thurtell MJ (2017) The yield of diagnostic imaging in patients with isolated Horner sSyndrome. Neurol Clin 35:145–151CrossRefPubMedGoogle Scholar
  147. 147.
    Maloney WF, Younge BR, Moyer NJ (1980) Evaluation of the causes and accuracy of pharmacologic localization in Horner’s syndrome. Am J Ophthalmol 90:394–402CrossRefPubMedGoogle Scholar
  148. 148.
    Davagnanam I, Fraser CI, Miszkiel K, Daniel CS, Plant GT (2013) Adult Horner’s syndrome: a combined clinical, pharmacological, and imaging algorithm. Eye 27:291–298CrossRefPubMedPubMedCentralGoogle Scholar
  149. 149.
    Sacco RL, Fredo L, Bello JA et al (1993) Wallenberg’s lateral medullary syndrome. Clinical-magnetic resonance imaging correlations. Arch Neurol 50:609–614CrossRefPubMedGoogle Scholar
  150. 150.
    Sadaka A, Schockman SL, Golnik KC (2017) Evaluation of Horner syndrome in the MRI era. J Neuroophthalmol 37:268–272CrossRefPubMedGoogle Scholar
  151. 151.
    Schievink WI (2001) Spontaneous dissection of the carotid and vertebral arteries. N Engl J Med 344:898–906CrossRefPubMedGoogle Scholar
  152. 152.
    Schievink WI, Mokri B, O'Fallon WM (1994) Recurrent spontaneous cervical-artery dissection. N Engl J Med 330:393–397CrossRefPubMedGoogle Scholar
  153. 153.
    Debette S, Leys D (2009) Cervical-artery dissections: predisposing factors, diagnosis, and outcome. Lancet Neurol 8:668–678CrossRefPubMedGoogle Scholar
  154. 154.
    Mokri B, Sundt TM Jr, Houser OW, Piepgras DG (1986) Spontaneous dissection of the cervical internal carotid artery. Ann Neurol 19:126–138CrossRefPubMedGoogle Scholar
  155. 155.
    Myles WM, Maxner CE (1994) Localizing value of concurrent sixth nerve paresis and postganglionic Horner’s syndrome. Can J Ophthalmol 29:39–42PubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of NeurologySankt Katharinen Hospital, Teaching Hospital of the Goethe UniversityFrankfurt am MainGermany
  2. 2.Department of Ophthalmology, NeuroophthalmologyGoethe UniversityFrankfurt am MainGermany
  3. 3.Institute of NeuroradiologyGoethe UniversityFrankfurt am MainGermany

Personalised recommendations