Pupillary sparing in oculomotor palsy from internal carotid aneurysm Case report
IRA KASOFF, M.D., AND DAVID L. KELLY, JR., M.D. Section on Neurosurgery, Bowman Gray School of Medicine of Wake Forest University, Winston-Salem, North Carolina
~" The authors report a patient with a carotid-posterior communicating artery aneurysm; although the oculomotor palsy accompanying such an aneurysm is almost universally recognized as being complete, with pupillary involvement, this patient had pupillary sparing in the absence of subarachnoid bleeding. A few similar cases have appeared in the literature. The mechanism of pupillary sparing appears to be based on the position of the parasympathetic pupilloconstrictor fibers within the subarachnoid portion of the third nerve and on the anatomic relationship between the third nerve and the junction of the carotid and posterior communicating arteries. KEY WORDS " intracranial aneurysm pupillary sparing
HE clinical presentation of oculomotor nerve palsy associated with an aneurysm of the internal carotid artery has been recognized since late in the 19th century. 2,8,5,g,11,13,1~,2~ The third nerve palsy is most commonly produced by a ruptured or nonruptured aneurysm at the junction of the internal carotid artery and the posterior communicating artery, a condition not characterized by pupillary sparing. Several authors ~,1~'~8'21 have stressed that the weakness must involve the pupilloconstrictor fibers of the oculomotor nerve. Indeed, Walsh and Hoyt 2a emphasized that an isolated oculomotor palsy with pupillary sparing will not usually occur as a result of intracranial aneurysm and stated that angiography should not be performed in such cases.
T
J. Neurosurg. / Volume 42 / June, 1973
9 oculomotor palsy
9
We are reporting the case of a patient with an oculomotor palsy and sparing of the pupil; he was subsequently found to have an internal carotid-posterior communicating aneurysm. We propose that this condition, although infrequent, can occur, and recommend angiography in cases where aneurysm appears likely. Case Report
A 54-year-old man developed a sudden, severe, right-sided, retro-orbital headache followed 3 days later by a drooping of the right eyelid and diplopia. He was admitted to the Neurosurgical Service of the North Carolina Baptist Hospital 7 days after the initial onset of pain. On physical examination, he demonstrated a marked ptosis of the right 713
I. Kasoff and D. L. Kelly, Jr. municating artery aneurysm that measured 5 mm in diameter, with a neck 4 mm long. The fundus extended posteriorly, inferiorly, and laterally (Fig. 2). A right frontotemporal craniotomy allowed excellent visualization of the aneurysm which had compressed the medial.aspect of the third nerve; no localized hemorrhage was found. The aneurysm was clipped at the neck. The operation was well tolerated and the patient was discharged on the 12th postoperative day. Within 2 months he had returned to work full time; by the end of 5 months, the third nerve palsy had completely cleared with no evidence of aberrant regeneration. Discussion In the presence of classical subarachnoid hemorrhage, the third nerve palsy lends itself FIG. 1. Upper: Photograph of patient showing to a fairly simple diagnostic exercise. unilateral ptosis from oculomotor palsy. Lower: However, when third nerve palsy occurs as an Patient looking to the left. Note equal pupils in the isolated lesion in an otherwise healthy inpresence of partial nerve palsy. dividual, we are faced with a greater spectrum of clinical possibilities. The exact frequency with which eye and extraocular muscle palsies of the oculomotor nerve palsy occurs with an unrupthird nerve (Fig. 1 upper). Both pupils were tured internal carotid-posterior comequal, n9rmal, and reactive (Fig. 1 lower). municating artery aneurysm is not known. In The cerebrospinal fluid showed no evidence of a highly detailed description of signs and blood; a 5-hour glucose tolerance test was symptoms of intracranial aneurysm, Walker 2~ normal. Cerebral arteriography revealed a cited a frequency range of 35% to 65% in all right internal carotid-posterior com- cases of unruptured supraclinoid aneurysms.
FI~. 2. Preoperative right carotid arteriogram showing the aneurysm. view. Right: Lateral view.
714
Left: Anteroposterior
J. Neurosurg. / Volume 42 / June, 1975
Pupillary sparing in oculomotor palsy Pool and Potts 17reported an over-all frequency of 78% from supraclinoid and intracavernous, and ruptured as well as unruptured aneurysms. Considering the reverse of the problem, Rucker, 18 in an analysis of 335 isolated third nerve palsies, found that aneurysms of the circle of Willis were the most common cause with an over-all frequency of 20%. Jefferson ~ had previously made a similar qualitative observation. The existence of an aneurysm in any location is most often heralded by subarachnoid hemorrhage. However, the importance of an oculomotor palsy as a first manifestation was illustrated by Okawara26 In his study on the warning signs preceding aneurysmal rupture, he found that extraocular muscle impairment was second in frequency to localized headache when the etiology was based on expansion of the aneurysm. However, when it occurs, the third nerve palsy may be an ominous sign of impending aneurysmal rupture. Extraocular muscle impairment preceded frank subarachnoid hemorrhage by an average of 29.6 days. Various authors, in discussing ocular findings associated with carotid posterior communicating artery aneurysms, have reported a small number of oculomotor palsies with pupillary sparing? ,4,1~ One may wonder whether pupillary sparing had occurred in other series of cases where ocular findings were not as well documented. The oculomotor nerve, in its subarachnoid portion, consists of a group of large caliber (10 to 16 ~) somatic fibers that innervate the extraocular muscles and the levator palpebrae superioris, and a group of smaller caliber (1 to 5 u) parasympathetic fibers that are destined for the ciliary ganglion25,~g Some investigators have also found sensory fibers that mediate the stretch reflexes in the extraocular muscles.~l. ~3 The location of the parasympathetic pupilloconstrictor fibers within the third nerve has been clarified through the investigations of Sunderland and Hughes a9 and Kerr and Hollowell. ~5 Sunderland and Hughes, working with cadavers, found that the small parasympathetic fibers were concentrated at the periphery of the superior aspect of the nerve just beneath the epineurium. Kerr and Hollowell, working primarily with dogs in experiments that included stimulation and transections of the J. Neurosurg. / Volume 42 / June, 1975
FI~. 3. Photomicrograph showing cross section of third nerve from a cadaver. Note smaller fibers concentrated in superior aspect of nerve. Bielschowsky's axon stain, • 200. third nerve, localized the pupillomotor fibers in the superficial dorsomedial arc of the nerve. In addition, by progressively transecting the fibers, beginning medially and moving laterally across the nerve, they found that a small number of pupillomotor fibers sometimes traveled in the lateral portion of the nerve, sufficient in number to maintain pupillary tone following ablation of the more numerous dorsomedially placed fibers. Kerr and Hollowell emphasized that these pupillomotor fibers are particularly vulnerable due to their location, as opposed to previous theories suggesting that these fibers are inherently more sensitive to pressure than other fibers. In cadaver studies of third nerves, we have confirmed the dorsoperipheral location of the small-caliber parasympathetic pupilloconstrictor fibers (Fig. 3). When seen on arteriograms, most carotidposterior communicating artery aneurysms are found to be directed posteriorly, inferiorly, and laterally. 2,9,13If we now consider the anatomic relationship between the oculomotor nerve in its subarachnoid course and the carotid-posterior communicating artery junction, it becomes apparent that 7]5
I. Kasoff and D. L. Kelly, Jr.
FIG. 4. Anatomical drawing showing relationship of the third nerve to the carotid artery and almost inevitable impingement of a carotid aneurysm (hatched areas) on the third nerve. (Reproduced by permission from Jefferson G: Isolated oculomotor palsy caused by intracranial aneurysm. Proc R Soc Med 40:419-431, 1947). many of these aneurysmal sacs will approach and impinge upon the nerve in its dorsomedial aspect (Fig. 4), thus illustrating the particular vulnerability of the pupilloconstrictor fibers in these cases. Aneurysmal involvement of the third nerve in the absence of frank subarachnoid hemorrhage most commonly occurs because of an acute aneurysmal dilation that may be accompanied by a small localized leakage. The nerve injury may be secondary to the dilation, the extravasation, or both. 2,1~ The phenomenon of pupillary sparing may be explained by the location of the parasympathetic fibers. In our case, we postulate the presence of a functional, laterally placed bundle of parasympathetic fibers, as described by Kerr and Hollowell,15 or an impingement of the aneurysm upon the third nerve which did not violate some more dorsally placed fibers. In other cases, the aneurysm may compress the nerve in an area relatively remote from the main concentration of parasympathetic fibers. Jefferson's description of internal carotid-posterior communicating artery aneurysms indicates that they may approach the third nerve inferiorly as well as superiorly24 The two other diseases most commonly considered in discussions of isolated thirdnerve palsy are diabetes mellitus and 716
ophthalmoplegic migraine. The clinical presentation of either disease may bear a striking resemblance to that of an internal carotid artery aneurysm, except for the more common demonstration of pupillary sparing in diabetes. The over-all incidence of ophthalmoplegia in diabetes is probably below 1%.2x The pathology of the diabetic oculomotor lesion has been located in the intracavernous portion of the nerve. Dreyfus, et al., 6 demonstrated extensive necrosis of axon cylinders and myelin sheaths of the larger fibers along the central axis of the nerve but not usually in the periphery; Asbury, et al., 1 demonstrated demyelinization in the same distribution. We can thus understand the pupillary sparing so commonly seen in this disease. However, in a study of 22 patients with diabetic ophthalmoplegia, Goldstein and Cogan 8 found five cases with pupillary involvement; it therefore appears somewhat inaccurate to attribute a pathognomonic quality to pupillary sparing or involvement. Ophthalmoplegic migraine has frequently been an area of some controversy. Its rarity is attested to by Friedman, et al., ~ who found only eight patients meeting the criteria of this disease from 5000 cases studied. The diagnosis of ophthalmoplegic migraine should be made only after all other possible J. Neurosurg. / Volume 42 / June, 1975
Pupillary sparing in oculomotor palsy structural causes have been eliminated. Because the clinical picture is so controversial, Walsh and O ' D o h e r t y 22 advocate angiography in these cases.
Conclusion After examining the underlying pathology and briefly looking at other nonsurgical diseases able to mimic the ophthalmoplegic presentation of an intracranial aneurysm, we urge a less rigid approach in weighing the importance of pupillary sparing. Because of the potential catastrophic consequences inherent in aneurysmal disease, we urge that aggressive diagnostic efforts, including angiography, be undertaken when intracranial aneurysm seems a likely diagnosis. The neurosurgeon who is able to approach a symptomatic intracranial aneurysm in the absence of frank subarachnoid hemorrhage will have a distinct advantage.
Acknowledgment We wish to express our appreciation to Dr. Nitya R. Ghatak of the Department of Pathology for his help with our exploration and demonstration of the third nerve in cadavers.
References 1. Asbury AK, Aldredge H, Hershberg R, et al: Oculomotor palsy in diabetes mellitus: a clinico-pathological study. Brain 93:555-566, 1970 2. Botterell EH, Lloyd LA, Hoffman H J: Oculomotor palsy due to supraclinoid internal carotid artery berry aneurysm. A long-term study of the results of surgical treatments on recovery of third-nerve function. Am J Ophthalmol 54:609-616, 1962 3. Cogan DG, Mount HTJ: Intracranial aneurysms causing ophthalmoplegia. Arch Ophthalmol 70:757-771, 1963 4. Dailey EJ, Holloway JA, Murto RE, et al: Evaluation of ocular signs and symptoms in cerebral aneurysms. Arch Ophthalmoi 71:463-474, 1964 5. Dandy WE: Intracranial Arterial Aneurysms. Ithaca, NY, Comstock Publishing Company, 1944 6. Dreyfus PM, Hakim S, Adams RD: Diabetic ophthalmoplegia. Report of case, with postmortem study and comments on vascular supply of human oculomotor nerve. Arch Neural Psychiatry 77:337-349, 1957 7. Friedman AP, Harter DH, Merritt HH: Ophthalmoplegic migraine. Arch Neural 7:320-327, 1962 8. Goldstein JE, Cogan DG: Diabetic J. Neurosurg. / Volume 42 / June, 1975
ophthalmoplegia with special reference to the pupil. Arch Ophthalmol 64:592-600, 1960 9. Harris P, Udvarhelyi GB: Aneurysms arising at the internal carotid-posterior communicating artery junction. J Neurosurg 14:180-191, 1957 10. Henderson JW: Intracranial arterial aneurysms. A study of 119 cases, with special reference to the ocular findings. Trans Am Ophthaimol Sac 53:349-462, 1955 11. H~55kO, Norl6n G: Aneurysms of the internal carotid artery. Acta Neural Stand 40:200-218, 1964 12. Hyland HH, Barnett HJM: The pathogenesis of cranial nerve palsies associated with intracranial aneurysms. Proc R Sac Med 47:141-146, 1954 13. Jefferson G: Isolated oculomotor palsy caused by intracranial aneurysm. Proc R Sac Med 40:419-432, 1947 14. Jefferson G: On the saccular aneurysms of the internal carotid artery in the cavernous sinus. Br J Surg 26:267-302, 1938 15. Kerr FWL, Hollowell OW: Location of pupillomotor and accommodation fibres in the oculomotor nerve: Experimental observations on paralytic mydriasis. J Neural Neurosurg Psychiatry 27:473-48 I, 1964 16. Okawara SH: Warning signs prior to rupture of an intracranial aneurysm. J Neurosurg 38:575-580, 1973 17. Pool JL, Potts DG: Aneurysms and Arteriovenous Anomalies of the Brain. Diagnosis and Treatment. New York, Harper & Row, 1965, p 83 18. Rucker CW: Paralysis of the third, fourth, and sixth cranial nerves. Am J Ophthalmol 46:787-794, 1958 19. Sunderland S, Hughes ESR: The pupilloconstrictor pathway and the nerves to the ocular muscles in man. Brain 69:301-309, 1946 20. Walker AE: Clinical localization of intracranial aneurysms and vascular anomalies. Neurology (Minneap) 6:79-90, 1956 21. Walsh FB, Hoyt WF: Clinical Neuroophthalmology. Baltimore, Williams & Wilkins, 1969, pp 1106-1114, 1763-1766 22. Walsh JP, O'Doherty DS: A possible explanation of the mechanism of ophthalmoplegic migraine. Neurology (Minneap) 10:10791084, 1960 23. Winckler G: Manuel d'anatomie topographique et functioneile. Paris, Masson et Cie, 1964, p 445 Address reprint requests to: Ira Kasoff, M.D., Section on Neurosurgery, Bowman Gray School of Medicine, Winston-Salem, North Carolina 27103. 717
IRA KASOFF, M.D., AND DAVID L. KELLY, JR., M.D. Section on Neurosurgery, Bowman Gray School of Medicine of Wake Forest University, Winston-Salem, North Carolina
~" The authors report a patient with a carotid-posterior communicating artery aneurysm; although the oculomotor palsy accompanying such an aneurysm is almost universally recognized as being complete, with pupillary involvement, this patient had pupillary sparing in the absence of subarachnoid bleeding. A few similar cases have appeared in the literature. The mechanism of pupillary sparing appears to be based on the position of the parasympathetic pupilloconstrictor fibers within the subarachnoid portion of the third nerve and on the anatomic relationship between the third nerve and the junction of the carotid and posterior communicating arteries. KEY WORDS " intracranial aneurysm pupillary sparing
HE clinical presentation of oculomotor nerve palsy associated with an aneurysm of the internal carotid artery has been recognized since late in the 19th century. 2,8,5,g,11,13,1~,2~ The third nerve palsy is most commonly produced by a ruptured or nonruptured aneurysm at the junction of the internal carotid artery and the posterior communicating artery, a condition not characterized by pupillary sparing. Several authors ~,1~'~8'21 have stressed that the weakness must involve the pupilloconstrictor fibers of the oculomotor nerve. Indeed, Walsh and Hoyt 2a emphasized that an isolated oculomotor palsy with pupillary sparing will not usually occur as a result of intracranial aneurysm and stated that angiography should not be performed in such cases.
T
J. Neurosurg. / Volume 42 / June, 1973
9 oculomotor palsy
9
We are reporting the case of a patient with an oculomotor palsy and sparing of the pupil; he was subsequently found to have an internal carotid-posterior communicating aneurysm. We propose that this condition, although infrequent, can occur, and recommend angiography in cases where aneurysm appears likely. Case Report
A 54-year-old man developed a sudden, severe, right-sided, retro-orbital headache followed 3 days later by a drooping of the right eyelid and diplopia. He was admitted to the Neurosurgical Service of the North Carolina Baptist Hospital 7 days after the initial onset of pain. On physical examination, he demonstrated a marked ptosis of the right 713
I. Kasoff and D. L. Kelly, Jr. municating artery aneurysm that measured 5 mm in diameter, with a neck 4 mm long. The fundus extended posteriorly, inferiorly, and laterally (Fig. 2). A right frontotemporal craniotomy allowed excellent visualization of the aneurysm which had compressed the medial.aspect of the third nerve; no localized hemorrhage was found. The aneurysm was clipped at the neck. The operation was well tolerated and the patient was discharged on the 12th postoperative day. Within 2 months he had returned to work full time; by the end of 5 months, the third nerve palsy had completely cleared with no evidence of aberrant regeneration. Discussion In the presence of classical subarachnoid hemorrhage, the third nerve palsy lends itself FIG. 1. Upper: Photograph of patient showing to a fairly simple diagnostic exercise. unilateral ptosis from oculomotor palsy. Lower: However, when third nerve palsy occurs as an Patient looking to the left. Note equal pupils in the isolated lesion in an otherwise healthy inpresence of partial nerve palsy. dividual, we are faced with a greater spectrum of clinical possibilities. The exact frequency with which eye and extraocular muscle palsies of the oculomotor nerve palsy occurs with an unrupthird nerve (Fig. 1 upper). Both pupils were tured internal carotid-posterior comequal, n9rmal, and reactive (Fig. 1 lower). municating artery aneurysm is not known. In The cerebrospinal fluid showed no evidence of a highly detailed description of signs and blood; a 5-hour glucose tolerance test was symptoms of intracranial aneurysm, Walker 2~ normal. Cerebral arteriography revealed a cited a frequency range of 35% to 65% in all right internal carotid-posterior com- cases of unruptured supraclinoid aneurysms.
FI~. 2. Preoperative right carotid arteriogram showing the aneurysm. view. Right: Lateral view.
714
Left: Anteroposterior
J. Neurosurg. / Volume 42 / June, 1975
Pupillary sparing in oculomotor palsy Pool and Potts 17reported an over-all frequency of 78% from supraclinoid and intracavernous, and ruptured as well as unruptured aneurysms. Considering the reverse of the problem, Rucker, 18 in an analysis of 335 isolated third nerve palsies, found that aneurysms of the circle of Willis were the most common cause with an over-all frequency of 20%. Jefferson ~ had previously made a similar qualitative observation. The existence of an aneurysm in any location is most often heralded by subarachnoid hemorrhage. However, the importance of an oculomotor palsy as a first manifestation was illustrated by Okawara26 In his study on the warning signs preceding aneurysmal rupture, he found that extraocular muscle impairment was second in frequency to localized headache when the etiology was based on expansion of the aneurysm. However, when it occurs, the third nerve palsy may be an ominous sign of impending aneurysmal rupture. Extraocular muscle impairment preceded frank subarachnoid hemorrhage by an average of 29.6 days. Various authors, in discussing ocular findings associated with carotid posterior communicating artery aneurysms, have reported a small number of oculomotor palsies with pupillary sparing? ,4,1~ One may wonder whether pupillary sparing had occurred in other series of cases where ocular findings were not as well documented. The oculomotor nerve, in its subarachnoid portion, consists of a group of large caliber (10 to 16 ~) somatic fibers that innervate the extraocular muscles and the levator palpebrae superioris, and a group of smaller caliber (1 to 5 u) parasympathetic fibers that are destined for the ciliary ganglion25,~g Some investigators have also found sensory fibers that mediate the stretch reflexes in the extraocular muscles.~l. ~3 The location of the parasympathetic pupilloconstrictor fibers within the third nerve has been clarified through the investigations of Sunderland and Hughes a9 and Kerr and Hollowell. ~5 Sunderland and Hughes, working with cadavers, found that the small parasympathetic fibers were concentrated at the periphery of the superior aspect of the nerve just beneath the epineurium. Kerr and Hollowell, working primarily with dogs in experiments that included stimulation and transections of the J. Neurosurg. / Volume 42 / June, 1975
FI~. 3. Photomicrograph showing cross section of third nerve from a cadaver. Note smaller fibers concentrated in superior aspect of nerve. Bielschowsky's axon stain, • 200. third nerve, localized the pupillomotor fibers in the superficial dorsomedial arc of the nerve. In addition, by progressively transecting the fibers, beginning medially and moving laterally across the nerve, they found that a small number of pupillomotor fibers sometimes traveled in the lateral portion of the nerve, sufficient in number to maintain pupillary tone following ablation of the more numerous dorsomedially placed fibers. Kerr and Hollowell emphasized that these pupillomotor fibers are particularly vulnerable due to their location, as opposed to previous theories suggesting that these fibers are inherently more sensitive to pressure than other fibers. In cadaver studies of third nerves, we have confirmed the dorsoperipheral location of the small-caliber parasympathetic pupilloconstrictor fibers (Fig. 3). When seen on arteriograms, most carotidposterior communicating artery aneurysms are found to be directed posteriorly, inferiorly, and laterally. 2,9,13If we now consider the anatomic relationship between the oculomotor nerve in its subarachnoid course and the carotid-posterior communicating artery junction, it becomes apparent that 7]5
I. Kasoff and D. L. Kelly, Jr.
FIG. 4. Anatomical drawing showing relationship of the third nerve to the carotid artery and almost inevitable impingement of a carotid aneurysm (hatched areas) on the third nerve. (Reproduced by permission from Jefferson G: Isolated oculomotor palsy caused by intracranial aneurysm. Proc R Soc Med 40:419-431, 1947). many of these aneurysmal sacs will approach and impinge upon the nerve in its dorsomedial aspect (Fig. 4), thus illustrating the particular vulnerability of the pupilloconstrictor fibers in these cases. Aneurysmal involvement of the third nerve in the absence of frank subarachnoid hemorrhage most commonly occurs because of an acute aneurysmal dilation that may be accompanied by a small localized leakage. The nerve injury may be secondary to the dilation, the extravasation, or both. 2,1~ The phenomenon of pupillary sparing may be explained by the location of the parasympathetic fibers. In our case, we postulate the presence of a functional, laterally placed bundle of parasympathetic fibers, as described by Kerr and Hollowell,15 or an impingement of the aneurysm upon the third nerve which did not violate some more dorsally placed fibers. In other cases, the aneurysm may compress the nerve in an area relatively remote from the main concentration of parasympathetic fibers. Jefferson's description of internal carotid-posterior communicating artery aneurysms indicates that they may approach the third nerve inferiorly as well as superiorly24 The two other diseases most commonly considered in discussions of isolated thirdnerve palsy are diabetes mellitus and 716
ophthalmoplegic migraine. The clinical presentation of either disease may bear a striking resemblance to that of an internal carotid artery aneurysm, except for the more common demonstration of pupillary sparing in diabetes. The over-all incidence of ophthalmoplegia in diabetes is probably below 1%.2x The pathology of the diabetic oculomotor lesion has been located in the intracavernous portion of the nerve. Dreyfus, et al., 6 demonstrated extensive necrosis of axon cylinders and myelin sheaths of the larger fibers along the central axis of the nerve but not usually in the periphery; Asbury, et al., 1 demonstrated demyelinization in the same distribution. We can thus understand the pupillary sparing so commonly seen in this disease. However, in a study of 22 patients with diabetic ophthalmoplegia, Goldstein and Cogan 8 found five cases with pupillary involvement; it therefore appears somewhat inaccurate to attribute a pathognomonic quality to pupillary sparing or involvement. Ophthalmoplegic migraine has frequently been an area of some controversy. Its rarity is attested to by Friedman, et al., ~ who found only eight patients meeting the criteria of this disease from 5000 cases studied. The diagnosis of ophthalmoplegic migraine should be made only after all other possible J. Neurosurg. / Volume 42 / June, 1975
Pupillary sparing in oculomotor palsy structural causes have been eliminated. Because the clinical picture is so controversial, Walsh and O ' D o h e r t y 22 advocate angiography in these cases.
Conclusion After examining the underlying pathology and briefly looking at other nonsurgical diseases able to mimic the ophthalmoplegic presentation of an intracranial aneurysm, we urge a less rigid approach in weighing the importance of pupillary sparing. Because of the potential catastrophic consequences inherent in aneurysmal disease, we urge that aggressive diagnostic efforts, including angiography, be undertaken when intracranial aneurysm seems a likely diagnosis. The neurosurgeon who is able to approach a symptomatic intracranial aneurysm in the absence of frank subarachnoid hemorrhage will have a distinct advantage.
Acknowledgment We wish to express our appreciation to Dr. Nitya R. Ghatak of the Department of Pathology for his help with our exploration and demonstration of the third nerve in cadavers.
References 1. Asbury AK, Aldredge H, Hershberg R, et al: Oculomotor palsy in diabetes mellitus: a clinico-pathological study. Brain 93:555-566, 1970 2. Botterell EH, Lloyd LA, Hoffman H J: Oculomotor palsy due to supraclinoid internal carotid artery berry aneurysm. A long-term study of the results of surgical treatments on recovery of third-nerve function. Am J Ophthalmol 54:609-616, 1962 3. Cogan DG, Mount HTJ: Intracranial aneurysms causing ophthalmoplegia. Arch Ophthalmol 70:757-771, 1963 4. Dailey EJ, Holloway JA, Murto RE, et al: Evaluation of ocular signs and symptoms in cerebral aneurysms. Arch Ophthalmoi 71:463-474, 1964 5. Dandy WE: Intracranial Arterial Aneurysms. Ithaca, NY, Comstock Publishing Company, 1944 6. Dreyfus PM, Hakim S, Adams RD: Diabetic ophthalmoplegia. Report of case, with postmortem study and comments on vascular supply of human oculomotor nerve. Arch Neural Psychiatry 77:337-349, 1957 7. Friedman AP, Harter DH, Merritt HH: Ophthalmoplegic migraine. Arch Neural 7:320-327, 1962 8. Goldstein JE, Cogan DG: Diabetic J. Neurosurg. / Volume 42 / June, 1975
ophthalmoplegia with special reference to the pupil. Arch Ophthalmol 64:592-600, 1960 9. Harris P, Udvarhelyi GB: Aneurysms arising at the internal carotid-posterior communicating artery junction. J Neurosurg 14:180-191, 1957 10. Henderson JW: Intracranial arterial aneurysms. A study of 119 cases, with special reference to the ocular findings. Trans Am Ophthaimol Sac 53:349-462, 1955 11. H~55kO, Norl6n G: Aneurysms of the internal carotid artery. Acta Neural Stand 40:200-218, 1964 12. Hyland HH, Barnett HJM: The pathogenesis of cranial nerve palsies associated with intracranial aneurysms. Proc R Sac Med 47:141-146, 1954 13. Jefferson G: Isolated oculomotor palsy caused by intracranial aneurysm. Proc R Sac Med 40:419-432, 1947 14. Jefferson G: On the saccular aneurysms of the internal carotid artery in the cavernous sinus. Br J Surg 26:267-302, 1938 15. Kerr FWL, Hollowell OW: Location of pupillomotor and accommodation fibres in the oculomotor nerve: Experimental observations on paralytic mydriasis. J Neural Neurosurg Psychiatry 27:473-48 I, 1964 16. Okawara SH: Warning signs prior to rupture of an intracranial aneurysm. J Neurosurg 38:575-580, 1973 17. Pool JL, Potts DG: Aneurysms and Arteriovenous Anomalies of the Brain. Diagnosis and Treatment. New York, Harper & Row, 1965, p 83 18. Rucker CW: Paralysis of the third, fourth, and sixth cranial nerves. Am J Ophthalmol 46:787-794, 1958 19. Sunderland S, Hughes ESR: The pupilloconstrictor pathway and the nerves to the ocular muscles in man. Brain 69:301-309, 1946 20. Walker AE: Clinical localization of intracranial aneurysms and vascular anomalies. Neurology (Minneap) 6:79-90, 1956 21. Walsh FB, Hoyt WF: Clinical Neuroophthalmology. Baltimore, Williams & Wilkins, 1969, pp 1106-1114, 1763-1766 22. Walsh JP, O'Doherty DS: A possible explanation of the mechanism of ophthalmoplegic migraine. Neurology (Minneap) 10:10791084, 1960 23. Winckler G: Manuel d'anatomie topographique et functioneile. Paris, Masson et Cie, 1964, p 445 Address reprint requests to: Ira Kasoff, M.D., Section on Neurosurgery, Bowman Gray School of Medicine, Winston-Salem, North Carolina 27103. 717
