Position and Vibration Sensations: Functions of the Dorsal Spinocerebellar Tracts? Elliott D. Ross, M D , Joel B. Kirkpatrick, M D , and August0 C. B. Lastimosa, M D

Clinical evidence is presented w h i c h establishes f o r t h e first t i m e t h a t position and vibration sensations may b e carried i n t h e dorsal spinocerebellar tracts. W e present a patient w h o incurred a spinal cord infarction e i g h t months prior to death that caused a Brown-SCquard syndrome w i t h loss of position and vibration senses i n t h e r i g h t lower extremity. The infarction spared the r i g h t fasciculus gracilis and t h u s supports t h e recent observations i n h u m a n beings (and animals) t h a t conscious proprioception is not a function of the dorsal columns. T h e vibratory a n d position losses were best correlated w i t h the portion of t h e lesion involving t h e r i g h t dorsal spinocerebellar tract. Arguments are furnished based o n physiological experiments i n animals that conscious proprioception may b e carried by Morin's spinocervicothalamic pathway, w h i c h forms part of the dorsal spinocerebellar tract in the spinal cord. Ross ED, Kirkpatrick JB, Lastimosa ACB: Position and vibration sensations: functions of the dorsal spinocerebellar tracts? Ann Neurol 5 : 17 1- 176, 1979

Certain clinical observations in humans IS, 15, 241 and recent neurobehavioral studies in animals [ 17, 18, 2 11 have undermined the classic dictum that position and vibration sensations are functions of the dorsal columns. The clinical findings in the BrownS6quard syndrome support the idea that conscious proprioception is conveyed ipsilaterally in the spinal cord. Although it is usually assumed that the position and vibratory deficits in a Brown-S6quard syndrome reflect a dorsal column lesion [2, 121, reports in the literature contain no pathological data to support this localization. In fact, the exact anatomical pathway (or pathways) subserving position and vibration sensations in the spinal cord of humans is, at present, unknown. With these points in mind we report the following clinicopathological analysis of a patient who sustained a Brown-Skquard syndrome eight months prior to death.

In April, 1076, a 57-year-old man was transferred t o the Dallas Veterans Administration Hospital from another hospital three weeks after sustaining a presumed anterior spinal artery occlusion. The patient was examined by one of us (A. C. B. L.) on admission and throughout his hospital stay. The general physical, language, and mental status examinations were normal. A right Horner syndrome was pres-

ent. There was mild weakness in the left arm, confined to the triceps, biceps, deltoid, and interosseous muscles, and moderate weakness of the right arm, greater distally, in a predilection pattern. The right leg was flaccid, with severe weakness proximally and complete paralysis distally. The left leg was mildly weak on hip flexion and ankle flexionextension. Reflexes were 2 + and equal in the upper and left lower extremities and 3+ in the right lower extremity. A right Babinski sign was observed. O n sensory examination (Fig 1) there was prominent loss of position and vibration sensations in the entire right lower extremity and severe diminution of pinprick and temperature appreciation in the entire left lower extremity t o approximately T12.A hyperesthetic response to pinprick was observed in the right lower extremity. The patient noted dpsesthesia, characterized as numbness to touch, over portions of his torso where light touch, pinprick, and temperature sensations were perceived normally. T h e patient's hospital course was uneventful. At discharge four weeks later, there was no significant change in his neurological findings except for increased right leg strength . T h e patient was followed in the neurology clinic, but none of the subsequent sensory examinations were done in sufficient detail to accurately assess and follow his sensory losses. In November, 1076, he was readmitted because of persistent left lower lobe pneumonia that proved to be secondary to an oat cell carcinoma. Radiation therapy was begun three weeks later, but the patient suffered a respiratory arrest and died the following day.

From the Departments of Neurology and Pathology, University of Texas Health Science Center, Dallas, TX. Accepted for publication June 20, 1978.

Address reprint requests to Dr Ross, Department of Neurology, University of Texas Health Science Center, 5 3 2 3 Harry Hines Blvd, Dallas, TX 7 5 2 3 5 .

Case Report

0364-5134/77/020171-06$01.25 @ 1978 by Elliott D. Ross

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Pathological Examination At autopsy, the brain and spinal cord were removed and fixed in 10% formalin. T h e spinal canal, epidural fat, anti spinal roots were examined in detail through a complete posterior laminectomy; no metastases were identified. The oat cell carcinoma was confined to the lung. The descending aorta and its branches showed moderately advanced atheroma formation. The brain and spinal cord were cut four weeks after fixation. They appeared normal on visual and tactile inspection except for focal atrophy and cyst formation at T,-Ts o n the anterior and central aspect of the spinal cord. The spinal cord was then divided inro segments at C2, C,, C,, C6, Clr CB,T,, T,. T,, T,, TI;, T,, TI,,,Ti,, L3, and S, and embedded in paraffin. Microscopic sections from each level were stained with cresyl violet, Bodian, and Weil stains. Figure 2 displays the histological findings in sections stained with Weil (myelin) stain at various spinal and medullary levels. The primary lesion was bilateral and extended from C, to T, with greater damage in the right half of the cord. At T, it affected the fasciculi cuneati, with mild extension into the extreme ventral portions of the fasciculi gracili. greater on the right than the left. The bulk of the fasciculi gracili, however, were spared. The gray matter and ventral white matter banking the ventral spinal fissure were involved bilaterally. T h e lesion extended into the middle and posterior portions of the right lateral funiculus but spared some of the more anterior portions. Above the primary lesion at C, there was ascending degeneration in the extreme portions of the right lateral white matter extending from the sulcus ventral lateralis to just short of the dorsal root entry zone. There was also bilateral, almost symmetrical degeneration in the medial portions of the dorsal columns, confined for the most part to the fasciculi cuneati. In the medulla, the right lateral ascending degeneration continued inro the brainstem, but a portion of it extended dorsally into the inferior cerebellar peduncle.

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Fig I . Sensorji map of our patient during initialrz~aluationat Dallas Veterans Administratiotz Hospital. Note the bilateral but asyvinietrical areas o f &se.rthesia without sensov?, loss oz?er the torso. The 1n.rse.r of position and r,ibration sensatinns ii'ere most profourid at the right toe.r, ankle, andknee. A hyperestheticresponse t o pinprick toas observed in the right lower extremity.

F i g 2. Spinal and medullary sections stairied for niyelin with Weil stain. The anatomic-a1left side of the spirial cord atid medulla is ipsiluteral t o the labeling irrdicatiwg t h e lez'el of the section (MM = mid medulla, LM = IOU' medulla. UPD = upper pyramidal decussation). The pen lznes encompass areas of necrosis, infarction. and degeneration as determined by microscopic examination. IN this figure the actual itifan-tion zs situated only at lezielc C , ( F i . T , (Gi. and T , ( H i , i d d e ascending degeneration is seen at leiiels AIM (A), LM (Bi. U P D (C) and C., ( D i .and descending degeneration at T,( I ) . The small black arzotos at the dorsal surface of the spinal r-ord (leiiels C,, C;, T I ,arid T,) point t o the dorsal intermediate siilcxs. which divides the fasciculus gracilis from the fasciculus runeatus. The diagram of C7 (Ei displays the location of the principal ascending sensory pathways in the spitial cord (left) and the approximate segniental layering of the fibers c0mpri.qing the dorsal columns (right), as derived,from data pnblished by Foerster [ 9 ] ,Carpenter [ 7 ] and , Walker and Weaver [221. One should be aware that as it ascends the reri,icadl cord, the fasciculus gracilis becomes wedge shaped. snialler. and confitled t o the dorsal portions of t h e dorsal columvi. Thirs, most of-the degevieration seen at C ( D i in the dorjal coliouns actually resides iti t h e fasi~iculuscurieatu.r (compare with C7;.see E. FI,

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Below the primary lesion at T8, descending degeneration was present in the right lateral funiculus and bilaterally in the ventral white marter on each side of the ventral fissure. Pathologically, the lesion was an infarct. The necrotic tissue had been completely resorbed except for a few remaining gitter cells. Hypertrophic fibrous astrocytes formed a loose glial scar in the damaged regions. The arteries of the spinal cord were fibrotic with intimal thickening, indicating the presence of arteriosclerosis; no vascular occlusion was seen.

Clinicopathological Correlations The lesion disrupted the following white matter tracts: the ventral corticospinal, ventrolateral vestibulospinal, ventral and medial reticulospinal, and ventral spinothalamic tracts bilaterally; the corticospinal, lateral spinothalamic, dorsal and ventral spinocerebellar, and rubrotegmentospinal tracts on the right side; and parts of the upper thoracic contributions to the fasciculi cuneati and parts of the lower thoracic contributions to the fasciculi gracili bilaterally. The distribution and severity of the extremity paralyses, the right Horner syndrome, and the loss of pinprick and temperature sensations in the left lower extremity were easily accounted for by the lesion. The problem we encountered was to explain the loss of position and vibration sensations in the right leg based on classic sensory localization. The small dorsal column lesion clearly was not responsible because i t was bilateral and spared the right fasciculus gracilis for the most part. The only portion of the infarction that correlated with the loss of conscious proprioception was the asymmetrical and ipsilateral lesion in the right lateral funiculus at C,, C,, and T , that caused ascending degeneration in the right dorsal and ventral spinocerebellar tracts. Since the ventral spinocerebellar tract is sectioned routinely during anterolateral cordotomy without leading to deficits in vibration and position sensations [19, 251, it would appear that the damage to the righr dorsal spinocerebellar tract was critical in our patient. The possibility exists, and is not ruled out by our case, that lesions in both the dorsal and ventrai spinocerebellar tracts are necessary for ipsilateral deficits in conscious proprioception. Vierck’s [2 I ] experimental observations in monkeys, to be amplified in the discussion, do not support this possibility, however. The dysesthesia experienced by the patient i n various portions of his torso without concomitant sensory loss on formal testing was best ascribed to the small bilateral dorsal column infarction. Anatomically, this lesion was located where the ascending fibers from the upper thoracic contributions to the fasciculi cuneati and the lower thoracic contributions to the fasciculi gracili reside [ 7 ] . Although Brown-S&quard believed that dorsal column lesions produce hyperesthesia 151, our clinicopathological analysis did not confirm this view since our patient demonstrated hyperesthesia (to pinprick) only in his right leg. Wall 1231 and Wall and Noordenbos [24]have noted, however, that 2 of their patients with dorsal column lesions complained of numbness i n portions of their body that showed n o elementary sensory loss on formal examination.

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Discussion From a series of meticulous surgical experiments in animals, Brown-Skquard [3-51 established that: (1) sectioning a single dorsal column does not cause loss of sensibility t o temperature, pain, touch, or galvanism; if anything, it causes increased sensibility ipsilaterally ; (2 ) hemisectioning the spinal cord produces a loss of sensibility in the contralateral limb or limbs, an increase in sensibility in the ipsilateral limb or limbs, and severe paralysis of the ipsilateral limb (limbs) below the lesion; and (3) longitudinal division of the lumbosacral spinal cord renders the hind limbs completely insensible without causing paralysis, thus proving that “sensory impulses” enter the cord and immediately decussate t o the opposite side. BrownSequard further established through clinicopathological correlation that his observations in animals also apply to humans [5]. It should be noted, however, that evaluation of position and vibration sensations was not part of t h e neurological examination in the mid 1800s, and this particular component of the Brown-Sequard syndrome was added at a later date by other neurologists. The exact origin of the teaching that vibration and position sensibilities are functions of the dorsal columns is difficult t o establish. As reviewed by Wall [23] and others [G, 151, it probably evolved from the observation that diseases causing degeneration of the dorsal columns, especially tabes dorsalis, are all associated with profound losses of conscious proprioception. Although it was well known by the late 1800s that tabes is primarily an affliction of the dorsal roots, this particular fact was overlooked, and the proprioceptive loss was attributed t o dorsal column degeneration. Since the axons of t h e dorsal columns are derived directly from the dorsal root ganglia, damage to t h e dorsal roots causes not only primary degeneration of the dorsal columns but also denervation without degeneration of ascending, second-order sensory pathways. Thus, attributing position and vibration sensations t o t h e dorsal columns was based o n misinterpretation of pathological data, since any o n e of t h e denervated secondary sensory pathways could just as well have carried the information rostrally. A number of recent publications have unequivocally established in both humans and animals that position and vibration sensibilities are not carried by the dorsal columns. Cook and Browder 181 surgically severed the ipsilateral dorsal column in 8 patients with unilateral chronic limb pain. N o n e of the subjects had either transient or permanent disturbance of vibration sensation, and none suffered a permanent loss of position sensibility after surgery. I n 1953, Netsky 1151 published an extensive clinicopathological study o n springomyelia. Six patients had had loss of vibra-

tion sensation with preservation of position sense during the course of their illness. Pathologically, the vibratory loss was best correlated with cavitation in the medial portions of the lateral funiculi, and Netsky concluded that vibration sensibility is not a function of the dorsal columns. Wall and Noordenbos [241 have recently published 3 cases of partial spinal cord transection in which lesions of the dorsal column did not give rise to losses of position or vibration sensibilities. Vierck [2 13 performed various spinal cord tractotomies in monkeys taught to discriminate joint position sense at the knee. He found that lesions confined to either the dorsal o r the anterolateral columns, or both, produce no change in position sensation. Lesions confined to a unilateral posterior quadrant or hemisection of the cord, however, cause a loss of position sensibility ipsilaterally, with only moderate recovery after prolonged retraining. When combined with a contralateral anterolateral column lesion, a unilateral posterior quadrant lesion causes total and permanent loss of position sensibility ipsilatera1 to the lesioned posterior quadrant. The critical experiment4estroying the posterior portion of the lateral column (and sparing the dorsal column) either alone or in combination with a lesion of the contralateral anterolateral column-was not done. Therefore, one cannot accept the first part of Vierck’s conclusion that position sensation in the monkey’s knee is mediated by: “1) the ipsilateral fasciculus gracilis; 2) the axons ascending the lateral funiculus which are uncrossed and posteriorly situated . . . ; and 3) decussated axons in the anterior portion of the lateral funiculus.” In two publications, Schwartzman and Bogdonoff (17, 181 demonstrated that monkeys trained to discriminate position and vibration sensations retam these abilities after dorsal column section. In order to explain these findings, Schwartzman and Bogdonoff [I81 suggested an alternative route for conscious proprioception: Morin’s spinocervicothalamic pathway. From neurophysiological studies in animals it has been established that Morin’s spinocervicothalamic pathway carries information about the sensations of touch [ 141, pressure [ 141, position [ 141, and vibration [ l ] to the contralateral sensory cortex. It originates from all segmental levels of the spinal gray matter, but most prominently from Clarke‘s column, as a second-order sensory pathway [ 10, 131. The bulk of the ascending fibers travel as part of the dorsal spinocerebellar tract and synapse in the lateral cervical nucleus, a slender column of cells located just lateral and ventral to the dorsal gray matter from C, to the lower medulla. This nucleus is well delineated anatomically in cats, less so in primates and humans

[ 11, 16, 201. The axons from the lateral cervical nucleus immediately decussate and course just lateral to the medial lemniscus, synapsing in the ventral posterolateral (VPL) thalamus. A fourth-order neuron from the VPL thalamus projects the information carried by Morin’s pathway to the sensory cortex. The importance of the case reported here lies with the demonstration that a loss of conscious proprioception was best correlated with a lesion involving the right dorsal spinocerebellar tract. This establishes for the first time clinical evidence to support the idea that vibration and position sensations may be functions of the dorsal spinocerebellar tracts, which contain the second-order sensory axons of Morin’s spinocervicothalamic pathway. The observation also reinforces previously established findings that position and vibration sensations are not functions of the dorsal columns.

Addendum We have corresponded with Dr Peter Nathan concerning Case 93 in the publication by Nathan and Smith [ 14a]. This patient underwent a right cordotomy, followed in 105 days by a left cordotomy, prior to death. On microscopic examination the entire right lateral funiculus. i d a d i n , : the dorsal spimrerebellar trai-t, was destroyed by the first cordotomy; the midventral portion of the left lateral funiculus and the ventral portion of the left ventral funiculus were destroyed by the second operation. N o loss of position or vibration sensibilities was observed by Dr Nathan. Thus, the neuroanatomy of conscious proprioception in the human spinal cord is complex and probably involves more than one tract. In view of Dr Nathan’s observation, perhaps the destruction of the right dorsal spinocerebellar tract in combination with the ipsilateral ventral funiculus and/or contralateral medial ventral funiculus was the cause of our patient’s loss of vibration and position sensations in his right lower extremity. The authors thank Dr Roger Rosenberg for his critical evaluation of the manuscript.

References 1. Anderson SA: Projection of different spinal parhways to the second somatic sensory area in the cat. Acra Physiol Scand 56 [SUPPI194]:1-74, 1962 7 Brodal A: Neurological Anatomy. New York, Oxford Uni-. versity Press, 1969, p 207 3. Brody 1A. Wilkins RH: Brown-Stquard syndromc. Arch Neurol 19:347-348, 1968 (translation of Brown-Stquard CE: D e la rransmission des impressions sensitives par la moelle epini6re. C R SOCBiol (Paris) 1:192-194, 1849) 4 . Brown-Sequard CE: Explication de I’hemiplegie croiste d u senriment. C R Soc Biol (Paris) 2:70-74, 1850 5 . Brown-Sequard CE: Course of Lectures o n the Physiology and Pathology of the Central Nervous System. Philadelphia, Lppincott, 1860 6 . Calne DB, Pallis CA: Vibratory sense: a critical review. Brain 89:723-746, 1966

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IMD: Human Neuroanatomy. Seventh edirion. Baltimore, Williams & Wilkins. 1376, p p 228-242 8. Cook AW. Drowder EJ: Funcrion of the posterior columns in man. Arch Neurol 12:72-79. 1965 9. Foerster 0: Symptomarologie der Erkrankungen des Ruckenrnarks und Seiner Werzeln: 111. D a s Hinrerstrangsystern: 1. Anatomischer ijberbllck, in Bumkc 0. Ibersrer 0 (eels): Handbuch der Neurolopie. Berlin, Springer. 1936. vol 5, p p 349 359 10. H a H, Liu C N . Organization of the spino-cervico-thalamic system. J C o m p Neurol 127:445-4'0. 1960 1 I . Ha H, Morin F: Comparative anaromical observations of the ccrvical nucleus, nucleus cervicalis lateralis, of some primates. Anat Rec 148:3'4-3'5, 1964 12. Haymaker W : Ding's Local Diagnosis in Neurological Diseases. St. Louis, Mosby. 1969. pp 89-91 13. hloriri F: A new spinal pathway for cutaneous impulses. Am J Physiol 183:245-.?52. 1955 14. Morin F. Kitai ST, Portnoy H.er al: Afferent projections t o the lateral cervical nucleus: a microelectrode stully. An1 J Physiol 2O4:667 -67 2, 1963 Ida. Nathan I'W, Smith MC: Effecrs of two unilateral cordoromies o n the motility of [he lower limbs. Brain 06:47 1 .$94, 1973 15. Netsky hlG: Syringomyelia. a clinicopathologic study. AMA Arch Neurcil Psychiatry 70:74 1-7'7. 1353 7. Carpenter

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16. Rexed B, Brodal A: T h e nucleus cervicalis lateralis. J Neurophysiol 14:399-407. 195 1 17. Schwartxnan RJ, Bogdonoff hlD: Behavioral and anatomical analysis of vibration sensibility. Exp Ncurol ?0:43-5 I , 1968 18. Schwartzman RJ. Dogdonoff MD: Proprioceprion and vibration sensihility discrimination i n the absence of rhc posterior columns. Arch Ncurol 20:349-353. 1969 19. Stookcy B: T h e managcmcrir of intractable pain by chordoromy. Rcs Puhl Assoc Rcs Nerv M m t Dis 23:416-433, 1943 20. Truex RC, Taylor MJ, Smythe MO, et al: T h e lateral cervical nucleus of cat. dog and man. J Comp Neurol 139:93-104. 1970 2 1. Vierck CJ: Spinal pathways mclliating limb position sense. Anat Rcc 154:43'. 1966 22. Walker A[:, Weaver TA: T h c topical organization and termination of the fibers of the posterior columns in Mucuiu m datta. J C o m p h'eurol '0:145-158. 19-42 23. Wall PI): T h e sensory an11 motor role of impulses travelling in the dorsal columns towards cerebral cortex. Brain 9J:505524, 1970 24. Wall PD. N(xirJenbos W: Sensory functions which rcmain in man after complete rransection of Jvrsal C O I U ~ I I I S . Brain 100:641-653. 1977 25. White JC, Sweet W H : Pain. Its Mechanisms and Neurosurgical Control. Springfield. IL, Thomas, 1055

Position and vibration sensations: functions of the dorsal spinocerebellar tracts?

Position and Vibration Sensations: Functions of the Dorsal Spinocerebellar Tracts? Elliott D. Ross, M D , Joel B. Kirkpatrick, M D , and August0 C. B...
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