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Figure 1.
External photograph of the patient with complete ptosis of the left eye.

External photograph of the patient with complete ptosis of the left eye.

Figure 2.
Complete third nerve palsy with pupillary involvement in the left eye.

Complete third nerve palsy with pupillary involvement in the left eye.

Figure 3.
Reflexive left upper eyelid elevation and lacrimation on proprioceptive stimulation of the left upper eyelid.

Reflexive left upper eyelid elevation and lacrimation on proprioceptive stimulation of the left upper eyelid.

1.
Yuzuriha  SMatsuo  KIshigaki  YKikuchi  NKawagishi  KMoriizumi  T Efferent and afferent innervations of Mueller's muscle related to involuntary contraction of the levator muscle: importance for avoiding injury during eyelid surgery. Br J Plast Surg 2005;58 (1) 42- 52
PubMedArticle
2.
Weir  CRKnox  PCDutton  GN Does extraocular muscle proprioception influence oculomotor control? Br J Ophthalmol 2000;84 (9) 1071- 1074
PubMedArticle
3.
Porter  JDBaker  RSRagusa  RJBrueckner  JK Extraocular muscles: basic and clinical aspects of structure and function. Surv Ophthalmol 1995;39 (6) 451- 484
PubMedArticle
4.
Ban  RMatsuo  KOsada  YBan  MYuzuriha  S Reflexive contraction of levator palpebrae superioris muscle to involuntarily sustain the effective eyelid retraction through the transverse trigeminal proprioceptive nerve on the proximal Mueller's muscle: verification with evoked electromyography. J Plast Reconstr Aesthet Surg 2010;63 (1) 59- 64
PubMedArticle
5.
Atasever  AÇelik  HHDurgun  BYilmaz  E The course of the proprioceptive afferents from extrinsic eye muscles. Turk Neurosurg 1992;2 (4) 183- 186
6.
Chee  EChee  S-P Subconjunctival injection of triamcinolone in the treatment of lid retraction of patients with thyroid eye disease: a case series. Eye (Lond) 2008;22 (2) 311- 315
PubMedArticle
Research Letters
June 2010

Proprioceptive Transient Elevation of Ptotic Eyelid and Lacrimation in Congenital Third Nerve Palsy: The Monosynaptic Stretch or Hoffmann Reflex Gone Awry?

Author Affiliations

Author Affiliations: Department of Ophthalmology, Guru Nanak Eye Centre, Maulana Azad Medical College, New Delhi, India.

Arch Ophthalmol. 2010;128(6):797-798. doi:10.1001/archophthalmol.2010.97

Although proprioceptive structures seen in antigravity muscles like jaw-closing muscles are lacking in levator palpebrae superioris muscle (LPSM), another antigravity muscle, Müller muscle (MM), may act like one for LPSM.1 We report stretch-induced ephemeral eyelid elevation of the completely ptotic eyelid followed by copious lacrimation in a girl with congenital third nerve palsy, speculate about the neuronal pathways, and educe its diagnostic and therapeutic implications.

Report of a Case

A 10-year-old girl had complete drooping of the left eyelid with the globe fixed in abduction (Figure 1). Her birth and family history were unremarkable. Aided visual acuity was 20/20 OD and 20/60 OS. An isolated left complete pupillary-involving third nerve palsy with no signs of aberrant regeneration was noted (Figure 2). On pulling the left upper eyelid margin down with her finger, her ptotic eyelid reflexively elevated by 6 to 8 mm, drifting back in 30 to 50 seconds. Profuse lacrimation followed (Figure 3 and video, http://www.archophthalmol.com). The pupil, other muscles supplied by the third nerve, and the contralateral eyelid were unaffected. The phenomenon could be repeated immediately thereafter and was not abolished by local anesthesia. There was no jaw wink or associated salivation. Results from the rest of the examination and magnetic resonance imaging of the brain and orbits were unremarkable.

Comment

Proprioceptive structures, muscle spindles, and palisade endings exist in the global but not orbital layer of human extraocular muscles. Distal myotendinous junctions, the areas traumatized in most strabismus procedures, are most richly endowed. The information they relay, however, remains controversial.2 Levator palpebrae superioris muscle lacks a global layer as well as proprioceptive structures.1,3 Its orbital layer has 2 types of muscle fibers. Most (80%) are fast-twitch, singly innervated, fatigue-resistant fibers and the rest (20%) are slow-twitch, multiply innervated, fatigable fibers.3 The latter likely have an MM-mediated proprioceptive role, reflexively contracting in response to voluntary contraction of the former.1,4,5 Intraoperative stretching of MM is known to induce ipsilateral or bilateral involuntary contraction of LPSM.1 Thick (proprioceptive) and thin (sympathetic) nerve fibers on proximal and distal MM are shown to pass through the palpebral lobe of the lacrimal gland to join the lacrimal nerve. Electrical stimulation of thick but not thin fibers consistently results in involuntary retraction of the upper eyelid (Hoffmann reflex).1 Ban et al4 electromyographically verified the presence of monosynaptic trigemino-oculomotor reflex ostensibly mediated via mesencephalic and central caudal nuclei of the fifth and third cranial nerves and speculated that it may account for inexplicable ptosis following trauma, surgery, or tumor removal in the aponeurotic area of LPSM. The horseradish peroxidase technique has shown that fibers from the oculomotor nerve entering the trigeminal (ophthalmic) nerve are afferent in nature.5 A hyperactive monosynaptic trigemino-oculomotor reflex resulting from stretch by multiply innervated slow-twitch fibers as elaborated earlier1,4,5 likely gave rise to sustained, fatigable eyelid elevation here.

As the proprioceptive fibers run through the lacrimal gland and nerve,1 the lacrimation that follows could be due to cross talk between proprioceptive or sympathetic fibers with secretomotor fibers from superior salivatory nucleus. Sparing of other extraocular muscles supplied by the third cranial nerve further buttresses proprioceptive underpinnings. Such a monosynaptic reflex, conterminous with a jaw-jerk reflex, is quite distinct from motor miswiring resulting in a jaw-winking phenomenon in congenital ptosis.

Proprioceptive ephemeral eyelid elevation and lacrimation induced by stretching of the eyelid (MM) has not been reported to our knowledge. The phenomena, harnessed and modulated pharmacologically, may have tremendous diagnostic and therapeutic potential in entities like dry eye, thyroid eye disease, ocular myasthenia, pathological eyelid retraction, acquired ptosis, eyelid trauma, surgery involving the LPSM aponeurosis, and numerous neuromuscular disorders. Alleviation of eyelid retraction in thyroid eye disease by triamcinolone acetonide injections in MM is a case in point.6

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Article Information

Correspondence: Dr P. K. Pandey, Department of Ophthalmology, Guru Nanak Eye Centre, Maulana Azad Medical College, New Delhi, Ne 110002, India (pkpandey_001@yahoo.co.in).

Financial Disclosure: None reported.

References
1.
Yuzuriha  SMatsuo  KIshigaki  YKikuchi  NKawagishi  KMoriizumi  T Efferent and afferent innervations of Mueller's muscle related to involuntary contraction of the levator muscle: importance for avoiding injury during eyelid surgery. Br J Plast Surg 2005;58 (1) 42- 52
PubMedArticle
2.
Weir  CRKnox  PCDutton  GN Does extraocular muscle proprioception influence oculomotor control? Br J Ophthalmol 2000;84 (9) 1071- 1074
PubMedArticle
3.
Porter  JDBaker  RSRagusa  RJBrueckner  JK Extraocular muscles: basic and clinical aspects of structure and function. Surv Ophthalmol 1995;39 (6) 451- 484
PubMedArticle
4.
Ban  RMatsuo  KOsada  YBan  MYuzuriha  S Reflexive contraction of levator palpebrae superioris muscle to involuntarily sustain the effective eyelid retraction through the transverse trigeminal proprioceptive nerve on the proximal Mueller's muscle: verification with evoked electromyography. J Plast Reconstr Aesthet Surg 2010;63 (1) 59- 64
PubMedArticle
5.
Atasever  AÇelik  HHDurgun  BYilmaz  E The course of the proprioceptive afferents from extrinsic eye muscles. Turk Neurosurg 1992;2 (4) 183- 186
6.
Chee  EChee  S-P Subconjunctival injection of triamcinolone in the treatment of lid retraction of patients with thyroid eye disease: a case series. Eye (Lond) 2008;22 (2) 311- 315
PubMedArticle
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