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Show ]. C1in. Neuro-ophth.,lnwl. 2: 13-18, IQ82. Atypical Oculomotor Paresis WALTER WARREN, M.D. RONALD M. BURDE, M.D. TERENCE C. KLINGELE, M.D. G. ROPER-HALL D.B.O.(T.) Abstract A series of patients is presented with partial oculomotor palsies. The accompanying signs of neurologic dysfunction are indicative of a mesencephalic lesion. The peculiar anatomy of the third cranial nerve permits one to infer precise localization of the lesions. The oculomotor nerve (third cranial nerve) originates in a complex multipolar nucleus which lies in the rostral portion of the midbrain at the level of the superior colliculus. Each muscle supplied by the third cranial nerve is subserved by an identifiable mass of cells defining a subnucleus (Fig. 1, 2, and 3). These subnuclei have a characteristic dorsoventral, as well as rostrocaudal, arrangement. All of the extraocular muscles are innervated ipsilaterally except for the superior rectus muscle, which receives fibers from the contralateral nucleus, and the levator palpebrae superioris which is bilaterally innervated. J The fascicular portion of the oculomotor nerve arises from the ventral side of the nucleus, and fans out during its descent through the median longitudinal fasciculus and the red nucleus, eventually penetrating the medial portion of the cerebral peduncles. The fibers emerge from the base of the mesencephalon as multiple rootlets in the interpeduncular fossa. The rootlets merge immediately to form a large trunk invested by pia, which travels downward, rostrally, and laterally passing under the superior cerebellar artery and over the medial inferior side of the posterior communicating artery before piercing the dura at the top of the clivus. The oculomotor nerve travels in the lateral wall of the cavernous sinus. Posteriorly, it lies superior to the trochlear nerve and the first and second divisions of the trigeminal nerve. It courses downward and anteriorly to assume a position inferior to the trochlear nerve. As it enters From the Departments of Ophthalmology (WW,RMB,TCK, GRH), Neurology and Neurological Surgcry (RMBI. Washington University School of Medicine. 51. Louis, M'''ouri. March 1982 Figure 1. SchcmJti( diJgrJm of J <ross scctlon of thc mcscn( ephalic-prctectal lunctlOn Jt thc rostrJI end "f thc third crJnlJI nerve nuclcus. At this level. thc ,nfcn,)r rcctu, (IR) subc,'mplc, of thc third nervc 15 isolJtcd Jnd thc Jntcnor fJsclculJr "utflow is intlmJtely JS5l\ciJted with the rcd nuclcus (RJ\:) and the substantlJ nigrJ (Sub Nig.). E- WI\; = Edinger- WestphJI nucleus. the orbit through the superior orbital tissure, it divides into two major divisions~: a superior division supplying the levator palpebrae superioris and superior rectus muscle, and an inferior division supplying branches to the medial and inferior rectus muscles as well .1S a branch to the inferior oblique muscle, which .1 Iso c.uries p.uasymp.lthetic efferents to the- ciliary ganglion. Oculomotor p..He;is is .1 commlln ne-uwlogic sign.'" 4 The paresis may be tot.lll)r parti.ll. A tl)tal oculomotor paralysis is characterized by a Cl~mplete ptosis of the eyelid with deviation of the eye outw.ud and dllwnw.ud .lCc,)mp.lI1ied by a dil.lted nonreactiv(' pupil. In th('se- c.lses, the integrity l~f the abduc('ns and twchle.n ne-rves C.lll be- demonstrat(' d by t('sting the eye movements llf e-.1(h eye individually (ductions). H the- involved eye moves laterally (abducts). the .lbduce-ns nerve is intact. If the eye intorts on attempted downgaze, the trochlear nerve is intact. Although the topographical localization of partial paresis of the oculomotor nerve is often difficult, it is generally accepted that isolated involvement of the third cranial nerve occurs posterior to 13 thr C,lVl'rnOUS sinus." An excl'pti\ln to this rule l'ccurs in L1Sl'S whl'rl' ,I divisi\1I1,11 pMc.,is is prrsl'nt:;~ indic,lting ,m ,lIltrrior C,lVcrnous sinus or orbit,ll Il'si\ln. A r,lthl'r sp\'l'illl' tvpc llf OcUlollHlt\lr 1110nop,lrl'sis llr pMti,11 p,lrl'.,i., "culnd,lry III intrill.,ic inv\ llvellwnt of thl' Illl'scnCCph,llonc,lI1 bc po.,tul,lted tIl \\Ccu r d Ul' t\I t hI' pl'CU IiM ,1 n,ltOI11 ie,ll ,I rr,mgcIllent lIt thl' \lCulOl1lotor nuclrar Clll1lplex and its t,lscicul.H \lutflowh A series of rccent C,lSl'S with the cliniLll signs lIt this vrry specific type \If partial ll(ldonwtor p,Hesis have been srrn in thr NeuroOphth'lll11llltlgy Consult Office at Washington Univprsity, ,1I1d they torm the substancr of this report. The findings in these cases .He most sdtisfdctorily expl,lined by the presence of a central lesion within the Ilucleus or contiguous to it. Clinical Investigation All of the patients had a thorough medical and neurological evaluation. A full neuro-ophthalmic examination, which included examination of ocul.H motility, visual fields, and the fundus, was performed whpre possible. The motility examination included tpsting of ocular ductions (range of eye movements in each eye alone), versions (range of eye movempnts in both eyps together), and vergences (convergence and divergence), as well as qualitative and quantitative measurements of the ocular deviation in various gaze positions. In most cases, this included the plotting of a muscle balance chart on the Hess screen. Case Reports C<lse 1 A 69-year-old white man suffered three separate neurologic episodes. In the first. he complained of the sudden onset (November 1970) of vertical and horizontal diplopia, which was diagnosed ,IS a right inferior rectus palsy. This was differentiated from a skew deviation by the marked spcondary deviation demonstrable on the Hess chart. Tensilt)n testing and .Hteriography were norm,ll. The diplopia resolved spontaneously over a 2-month period. Seven months later, the patient developed balance difficulty and blurred vision relieved by (Overing one eye. Skull films, lumb,H puncture, ,1I1d ,111 other trsts were negJtive. Two weeks latpr, he developed d recurrence of his right inferior rectus pJresis, ,1l1d a resting Jnd intention tremor of the left Jrm WJS noted by one examiner. He sh\lwed ,1 tendency to deviatp to the Ipft whilr walking. No othrr long motor tr,lct signs could bc drnwnstr,ltrd. A right carotid ,Hteriogr,lm showed ,1therII11l,ltous ch,lI1ges in the right innominJtc ,1I1d intern,ll c,lwtid ,Htery. The Jir1opi'1 W,l" rplievpd bv a prism,ltic correcti\~n in hi"\',1.1.",/,,, Comment: This case probably represents an incomplete form of a ventral medial midbrain syndrome (i.e., Benedikt's syndrome),~J caused by a small bJsilJr artery branch occlusion (Fig. 1). C<lSC 2 A 5 I-ypar-old left-handed, white man was evaluJted approximJtely 2 years after the sudden development of ,1 right hemiparesis and tremor, concomitJnt with the onset of episodic obscurations of vision. These transient obscurations of vision occurred in the right visual field and lasted appoximately 30 minutes He described these epidsodes as "similar to looking at a jellyfish." Visual field testing failed to reveal a defect. He did not spontaneously complain of double vision, and in the straight-ahead position only an exophoria was noted. However, diplopia could be produced when the patient was asked to look down and to the left, compatible with a left inferior rectus paresis. This was quantitatively established on the Hess chart. This partial paresis had remained stable when the Hess chart was repeated 6 months later. Neurological examination demonstrated a resting tremor of about 7-8 movements per second of the wrist and elbow joints on the right side. This tremor was also present on finger-to-nose testing. A similar tremor, but of lesser magnitude, was noted in the right leg. Mild cogv"heel rigidity of the right wrist was present. No rhythmic movements of the palate or eyes were noted. The pupils were round and equal in diameter and reacted normallv. Diastolic blood pressure varied around 90 mm Hg. Laboratory results reflected .1 hyperlipidemia with a cholesterol of 37b mg/100 ml, and .1 triglyceride l,f 2b3 mg/100 ml. with a fasting blood sug.u of 08 mg/lOO ml. His cerebrospinal fluid protein W.lS -l8 mg/ 100 ml with a 6.1% gamma globulin fraction. Brain scan and computerized a,iJI tomography were normal. Comment: A clinical diagnosis was made of a non progressive lesion. .1 presumed infarction, in the left midbr.lin. which affected: 1) the red nucleus or brachium conjunctivum, or both, producing a midbrain tegmental tremor; 2) the substantia nigra producing cogwheeling rigidity; and 3) the rostral portion of the oculomotor complex producing a left inferior rectus paresis. The complaint of vague visu,ll illusions occurring in one hemifield is compatible with the diagnosis of intermittent posterior cNebr,ll insufficiency (Fig. 2). elSe 3 A 23-ye.lr-old woman complained of diplopia for the first time on her 14th hospital admission for multiple sclerosis. She was found to have an isolated left inferior rectus paresis. In addition to this physical finding, she had numerous central Journal of Clinical Neuro-ophthalmology O~edUC' IRS~R O!:,.evotor 10 MR" I ~MLF D*~ Figure 2. Sl'hl'mJtil' dIJ!\r.m, "f J l'rll'S sedil'" llf the mesenl'ephJllln Jt the l'JudJI end "f the third l'rJniJI nerve nudeus. emphJsizin!\ the junction "f the prJchium conjundivum (Be). the red nucleus (RN). Jnd the relJti,'nship t,) the supstJntiJ nigrJ (5. nigrJel Jnd the l'llmp,ments llf the third nerve nucleus. 5R = superior rectus subnucleus; IR = inferior rectus subnucleus; 10 = inferior obliljue subnucleus; MR = med'JI rectus subnucleus; MLF = mediJn longitudinJI fJsciculus. neurological signs which had been noted on previous admissions: specifically, quadriparesis, dysarthria, emotional lability, bilateral extensor responses, and ankle clonus. Her cerebrospinal fluid protein was 68 mg/100 ml with 17.2% gamma globulin fraction, and a colloidal gold curve of 442,210,000. Comment: It is proposed that an acute demyelinating lesion in the region of the rostral lateral portion of the left oculomotor nuclear complex produced her inferior rectus weakness. Case 4 A 66-year-old white woman complained of a sudden onset of vertical diplopia. Examination, including Hess chart evaluation, demonstrated bilateral inferior rectus weakness, greater on the left, and in addition, weakness of the left superior rectus muscle. The patient is an insulin-dependent diabetic individual and is also hypertensive, requiring the use of alpha-methyl dopa. She had a normal neurologic examination with the exception of the ocular motility disturbance. On a subsequent Hess chart examination 1 year later, the bilateral inferior rectus weakness was found to be unchanged. Comment: According to Warwick's scheme, the patient had a central infarction in the middle anterior portion of the oculomotor nucleus, greater March 1982 on the right side, producing a bilateral inferior rectus weakness, and a unilateral superior rectus weakness (Fig. 3). Case 5 An 18-year-old white girl suddenly developed diplopia and ataxia 1 week prior to admission to the hospitdl. Concomitdntly, she noted d sensation of her right ear being "plugged up." An otolaryngologist made the diagnosis of right otitis media and prescribed .lmpicillin. TWl) weeks prior tl) ddmission, a dental extraction W.1S perfl)rmed under generdl anesthesia .md was reportedly .lssociated with a dental abscess .md fever. During physical examination on admission, the patient had a Weber audiological finding th.1t 1.1teralized to the left side .1I1d .111 .lbsence of ocul.Jr responses to cold c.lloric stimuLltion in the right ear. Dysmetri.l of the right c'\tremities, .lbsent Pl)sition, .md decre.lsed vibration sens.1til1n of the left leg, and bilateral flexor pl.mt.u responses were noted. Oculdr motor examindtion revedled d horizontal, left-beating jerk nystagmus dnd a right inferior rectus and left superior rectus weakness that was qUdntitated by d Hess chdrt. There were so mononuclear leukocytes in the cerebrospindl fluid, Protein and gdmma globulin frdction were 15 Atvril"lll kllll\nllllor I'.Ht'sis Figure 3. SchemJt,c d'Jl(rJm of.\ u,,,,·,ecl,un "f the me,en«'phJlun Ihr,>ul(h the middle third uf the third ([In'JI nerve nUL leu .. Ic,R = "upenl>r reclu" ....ubnUl.... I('u~; IR = mfc-ri\.H redu~ ':-oubnudeu~. R\: = rC'd nu<.!c-u .... S nl~r.)(' := "ub... t.lntiJ nlgr.l). A (('ntrJlly Ji..l(Jlcd 1(,~lon ('''t('nJlfl~ trl'm the rl).:..trJI end uf Iht' third nerve nudl.'us cl.'ntrJllv With J b'JS tl> Ihl.' nl(ht eJudJllv I'l.'l.' F'l(. I, wlluld producl.' the bdJterJI ,nfenor reclus pJISIes Jnd the left superll" rectus pJres" notl.'d In (J,e 4. S,mdJrlv. J undJterJI leSiun l'n the nl(hl "Idl.' would producl.' the ri~hl inferior reclus pJlsv Jnd left .. uper,,>r rl.'ctus pJI ..v nL)led In (..15(' 5. normal. The patient was treated with intravenous ACTH drip and improved. Comment: A diagnosis of an inflammatory, probably demyelinating, process affecting the brainstem was made. There were probably multiple lesions. Specifically, one of the lesions probably affected the right side of the midbrain with involvement of the right oculomotor complex in its middle third, resulting in dysfunction of the right inferior rectus nuclear subcomplex (a right inferior rectus wea knessJ, and the right superior rectus nucle.u subcomplex (a left superior rectus weakness) (Fig. 3). Discussion Precise topographical IO(.lliz.ltion llf lesilms involving the 'lCulomotor nerve, either peripher.ll1y or centrally, is quite possible when thl'rl' are .1(companying neurologic signs. If thl' neurologi( deficit is .m isolated dysfun(tion of the o(ullll11lltor outflow, tl1pogr.lphi( loe.lliz.ltion llf the C.1Us.llive lesion may be inferred, in Sllme e.lses, from the particul'H ,m,llomy of the tol,ll OCUllll11lltor (lll11plex (i.e., nudeu<;, f.lSeiculus, nerves, .md divisions). A lesion ill the ,1llterior e,1VernllLIS sinus or "rI'lt ",,,,,1.1 1)(' '-'I""' tl-d t<l pn1due(' division.ll in-volvement. while isolated lesions of the inferior rectus. or the inferior rectus and contralateral superior rectus, could be assumed to be nuclear or fascicular in origin. In addition. incomplete oculomotor paresis may have its basis in differential involvement of nerve fibers within the main oculomotor trunk. For e"\ample. the pupillary fibers are known to lie superficially within the nerve and tend to be involved early in compressive lesions, and are often spared in ischemic lesions such as those associated with diabetes mellitus. The (entr.ll .m.ltomical arrangement of the ocuIOml) tor comple"\ permits discrete involvement of the inferil)r rectus subcomplex. According to Warwick. 1 the inferil)[ rectus subcomplex extends rostrally li\..e .1 peninsula. Thus, the inferior rectus nuclei ,1t the most rostral level of the oculomotor comrle"\ .He isolated (Fig. 1). A discrete lesion of the lleuloml)tor nucleus, or contiguous to it at its nwst wstral extent, can produce an isolated inferior rectus palsy. Similarly, a small midline lesion at this level can produce bilateral inferior rectus weakness. The first nuclear subcomplex adjacent to the inferior rectus subnucleus caudally controls the contralateral superior rectus muscle. A lesion slightly caudal to one producing an isolated inferior rectus palsy can affect the inferior and superior Journal of Clinical Neuro-ophthalmology W.lrr('n, BurdC', Klingel(', Roper-Hall Figure <I. Schematic di.lgr.lnl llf .1 S.lgllt.ll section of the upper brainstem emphaSizing the relationship elf the third rranlalnerve nudeus (llIL tll the red nudeus (RNL .lnd the brachium conlunctivum (BC). rectus subnuclei producing an ipsilateral inferior and contralateral superior rectus paresis (Fig. 3). It is our contention that the cases reported in this paper, isolated inferior rectus weaknesses (cases 1, 2, and 3), bilateral inferior rectus weakness and unilateral superior rectus weakness (case 4), and isolated inferior rectus and contralateral superior rectus weakness (case 5), are due to a focal central nervous system lesion, most likely involving the oculomotor complex at its rostral end. The associated physical findings as outlined in some of the cases help to place the causative lesion within the brainstem. The presence of a tremor in two of the five cases (cases 1 and 2) requires elaboration. It is well known that the combination of a motility disturbance in the distribution of the oculomotor nerve of one eye with a contralateral tremor comprises Benedikt's syndrome. lo Walsh and Hoytil suggest that the accompanying oculomotor dysfunction is total paresis. Our cases are unusual in that the oculomotor disturbance does not affect all oculomotor nerve function, just the inferior rectus portion. One of our cases (case 2), had a tremor present both at rest and on movement, thus fitting neither the classic resting nigra striatal tremor nor the intention cerebellar (or cerebellar outflow) tremor. According to Dejong, I~ this combination of tremor at rest and on movement is the feature of a rubral tremor. A tremor due to a lesion involving the brachium conjuctivum is present only on movement according to Cooper. I : 1 (See Figs. 2 and 4 for relationships of these structures to the oculomotor complex.) However, unanimity of opinion with respect to this point does not exist. Alpers '4 indi- March 1982 cates that the terms rubral and brachium conjunctivum are interchangable in describing a midbrain tegmental tremor. Thus, it does not appear to be established from the literature whether the tremor of Benedikt's syndrome is due to a lesion in the red nucleus alone, or in the brachium conjunctivum alone, or both. In any event, a single lesion could involve the rostral portion of the oculomotor complex where the inferior rectus alone is represented, and either the red nucleus IC•. In or the brachium conjunctivum 17 (Figs. 2 and 4). The combination of an inferior rectus weakness accompanied by a contralateral resting, and intention tremor may be more common than is reported or actively noted. The relative infrequency of this association is due to the lack of detailed ocular motility analysis in patients in whom a tremor is noted. We propose that any patient with .1 unilateral tremor present both at rest and on intention should be neuro-ophthalmologically evaluated for a subtle motility disturbance. The presence of signs indicating accompanying oculomotor dysfunction c.m provide a precise pathologic localiz.1tion of the lesion, and thus .1 better underst.mding of the underlying pathophysiolL)gy. References I. Warwick, R.: Represent.ltion of the extraocul.Jr muscles in the llCuloml)tor nuclei of the monkey. T. Compo Nl'urol. 98: 44Q-503, \Q53. 2. Fallopius, C.: Observationl's Anatomical'. Venice, 156\, pp 137-154. (As quoted by Susac and Hoyt in reference 7.) 3. Rucker, C.W.: Paralysis of the third, fourth, and 17 Alvpir.lllkulllnllllllr l'.Hesis s"lh rr.lIli.ll nerve,. Am. I l Jphth.linwl. 46: 7577< 1.t, 1<155. .t. Rutl,er, C.W.: The l.llISl', Ill' paLllysis Ill' the third, fllurth, .1Ilel sixth rr.lIli.ll nerVI',. Am. I ()phth.llm"l. td: 12<1,,-/2<15, I<1Nl. 5. W.11,h, I".K., .1Ilel flllyl, W.I'.· Clinic.1i N,'uro-Oph. th.J/nll''''gv ( Vol. I.). Willi.lIn, & Wil "ins, B.lltimore, p.l('lll, p. 252. tl. Rllper-H.III, C, .11lc! Burde, R.M.: Inferillr rer/us p.llsies .15 .1 1ll.lllifest.ltillll Ill' .1typic.11 IlIrd cranial nerve dise.lse. Am. ()rthopt. I 25: 122-130, 1975. 7. SUS.ll, I.U., .mel Hllyl, W.F.: Inferillr brJIKh palsy of th.. ocullll1llltor Ilerve. Ann. Npurol. 2: 330-330 , 1<177. 1'>. Walsh, FB., and Hllyt, W.F.: Ref. 5, p. 250. (l. W.Ilsh, F.B., and Hoyt, W.F.: Clinical Neuro-Ophth. Jlnwlclgv ( Vol. 2). Williams & Wilkins, Baltimore, ((lb(l, p. 11'>.t.t. 10. Wlllf, '.K.: The classical brain stem syndromes. In Tr.lIlslaticlns of the OriginJI Papers with Notes on E\'o/ution of Clinical NeuroanJtomy. ChJs. C Thomas, Springfield, 111.,1971, ChJpter6 (Benedikt's syndrome), originJI article by M. Benedikt. 11. Walsh, F.B., and Hoyt, W.F.: Ref. 5, p. 248. 12. Dejong, R.N.: The Neurologic EXJminJtion (3rd ed.) : ...: Hoeber, New York, 1967, pp. 210 and 539. 13. Cooper, 1.5.: Involuntary Movement Disorders. Harper & Row, New York, 1968, p. 118. /4. Alpers, B.L and MJncall, E.L.: Clinical Neurology (oth ed.). F.A. Davis, Philadelphia, 1971, p, 215, IS. Olszewski, J., and BJxter, D.: Cytoarchitecture of the Human Brain Stem. J.B. Lippincott, Philadelphia, 1954, p 132, 10. Singer, M., and YJkolev, P.E.: The Human Brain in S.Jgittal Section Chas. C Thomas, Springfield, III., 1954. 17. Rand, R. W.: An anatomical and experimental study of the cerebellar nuclei and the efferent pathways in the monkey. J Compo Neurol. 101: 167-223, 1954. Acknowledgment ThIS work was supported in part by a grant from Research To Prevent Blindness, Inc, New York, New York (Department of Ophthalmology). Write for reprints to: Ronald M. Burde, M.D., Department of Ophthalmology, Box 8090, 660 South Euclid Avenue, 51. Louis, Missouri 03110. Journal of Clinical Neuro-ophthalmo)ogy |
