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An Anatomical and Experimental Study of the Cerebellar Nuclei and Their Efferent Pathways in the Monkey

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An Anatomical and Experimental Study of the Cerebellar Nuclei and Their Efferent Pathways in the Monkey AN ANATOMICAL AND EXPERIMENTAL STUDY OF THE CEREBELLAR NUCLEI AND THEIR EFFERENT PATHWAYS IN THE MONKEY ROBERT WHEELER RAND Laboratory of Comparative Neurology, Department of Anatomy, Udversity of Miohigan, Ann Arbor FIFTEEN FIGURES INTRODUCTION Since the middle of the 19th century the extensive works and resultant discoveries of anatomists and physiologists have been unveiling the architecture and functions of the primate cerebellum with its associated nuclei and efferent tracts. Today the general concensus is that the cerebellum is con- cerned with the coordination of voluntary and/or involun- tary action of striated musculature or, as Tilney ('19) expressed it, the production of synergia between agonistic and antagonistic muscle groups. The distribution pattern of the efferent fibers of the cerebellar nuclei affords an anatomi- cal foundation for the interpretation of this functional or physiological result. These efferent fibers, which leave the cerebellum predominantly through the superior cerebellar peduncles, but also by way of the restiform bodies, terminate directly or indirectly in association with the motor pathways of vestibular, tegmental, tectal, pallidal, striatal and cortical origin. The present investigation was undertaken with the sup- position that this pattern of distribution to motor centers, or correlating areas, is the predominant cerebellar pattern and that the efferent fiber systems from the primate cere- 167 168 ROBERT WHEELER RAND bellar nuclei should be intimately related with all important extrapyramidal motor systems of the central nervous system. Among other new connections, it has been possible to find those of the cerebellum with the nuclei of such extrapyramidal systems as the medial longitudinal fasciculus and the dorsal longitudinal f asciculus. The author wishes to express his sincere appreciation to Professor 'Elizabeth C. Crosby under whose guidance and unending assistance this study was planned and executed. He is grateful to the sponsors of the Alphonso Morton Clover Medical Research Fund and the Otolaryngological Research Fund of the University of Michigan Medical School which financed this investigation. MATERIAL AND METHODS The species of monkeys used for the experimental portions of this study were Macaca mulatta and Macacus cynomolgus. Although 7 animals were experimented upon, only 4 are re- ported herein; the remaining three died of a dysentery (with which many monkeys are infected on arrival in this country) shortly after the operation. The normal anatomy of the cerebellar nuclei of Macaca mulatta was reviewed in prepa- rations from the Huber Comparative Neurological Collection stained by the Weil method ( '45) and the Huber modification ( '27) of the toluidine blue technique. The experimental ma- terial was prepared by the Marchi method using the Swank and Davenport ( '35) modification. The utilization of this technique affords only visualization of degenerating mye- linated fibers. All fibers become amyelinated at some distance proximal to their termination, a fact which must receive consideration in drawing conclusions. In series one, two and three a suboccipital craniectomy was performed aseptically under intravenous pentothal and/ or ether anesthesia. The size of the exposure varied. The dural incisions were closed whenever possible and the sub- CEREBELLAR NUCLEI AND CONNECTIONS 169 occipital musculature and fascia tightly approximated in anatomical layers to provide protection before suturing the skin. The McCulloch stereotaxic instrument was used in series 4 after aseptically making appropriate trephines un- der ether anesthesia. The lesions of the deep cerebellar nuclei and the superior cerebellar peduncles were produced by an insulated needle through which a mild cauterizing electric current was passed. In all instances preoperative and postoperative testing of the animals was carried out and included examination of the reflexes, the muscle tone, the cranial nerves, and the ability of the monkey to perform gross and fine movements of the trunk and extremities. All the monkeys presented here were sacrificed between the 14th and 20th postoperative days. After inducing surgi- cal anesthesia with ether, their thoracic cavities were rapidly opened bilaterally and their arterial systems perfused with 500 to 1,000cm3 of 10% formalin. The brains with attached cervical cord were removed carefully; in all instances the fixation was excellent. EXPERIMENTAL ANIMALS Mordcey I The subject of this experiment was a normal Macacus cynomolgus male of 44 pounds (2.0 kg) . On October 1, 1951, under ether anes- thesia, a bilateral suboccipital craniectomy was performed with direct exposure of the vermis and the medial portions of both cere- bellar hemispheres. The exposed cerebellum appeared normal. A slim electrode needle, insulated except for the tip, was inserted into the right side of the pyramis and directed into the right nucleus fastigii ; 3.5 milliamperes of electrical cauterizing current were passed through this needle for 30 seconds before it was removed. No gross blepding occurred. Recovery from the operation was unevent,ful, and immediate postoperative testing revealed occasional nystagmoid movements on right lateral gaze. On subsequent postoperative examinations over the next 14 days nystagmus was not evident on conjugate gaze in any direction. Nystagmus could not be produced even though the monkey was revolved rapidly, first to the left and then to the right, with his head in a horizontal plane. The extraocular muscles showed neither 170 ROBERT WHEELER RAND paralysis nor paresis, and reflex and voluntary conjugate gaze were normal in all spheres. The muscular tonus in tshe extremities re- mained normal, as did the deep tendon reflexes. The monkey was able to run, climb and jump well. He showed no evidences of cere- bellar disturbance, except for moderate retropulsion during the first 24 hours. Examination of the cranial nerves revealed nothing unusual. Stimulation of the plantar surface of the feet evoked no pathological response. After sacrificing the monkey on October 15, inspection of the brain showed the exterior of the cerebellum, cerebrum and brain stem to be normal except for a 5mm circular area of yellowish discoloration on the surface of the pyramis of the vermis, the site where the insulated electrode had been inserted. There was neither intracerebellar hemorrhage nor infection of the wound. The lesion (figs. 1, 2 and 3) as studied in Marchi preparation is small and localized. It begins at the most caudal end of the right nucleus fastigii involving the medioventral quadrant of that nucleus and also the inferior cerebellar commissure. As the lesion is followed rostrad, the medial half of the posterior third of the nucleus is included; at this level the lesion attains its maximum size (fig. 2). It then decreases in area, and, in the middle third of the nucleus is present only in the medioventral quadrant (fig. 3). At the junc- tion of the rostral and middle thirds of the nucleus fastigii the lesion ceases leaving the rostral third of the nucleus uninvolved. The degenerated fibers leave the right nucleus fastigii by several clear-cut routes. The greatest number first turn direetly dorsad, par- tially through the nucleus but especially along its medial border ; upon reaching the dorsal surface of the nucleus they arch sharply laterad, to the left and right, dispersing cephalad in the medullary stratum dorsal to the interpositus nucleus and dorsolateral to the dentate nucleus on either side (figs. 2 and 3), but with more crossed than uncrossed fibers. This pattern can be observed at all levels of the lesion. Within the cerebellum, from the ventral surface of the right nucleus f astigii, degenerated fascicles stream ventrolaterad to the right and left beneath the interpositus and dentate nuclei (fig. 1) to enter the floccular lobe on either side. They are particularly numerous and evident on the side of the lesion, and are limited exclusively to these lobules. Mortkey II This macaque (Macacus mulatta) was a healthy, normal young female weighing 5 pounds (2.25 kg). On September 27, 1951, a left subocoipital craniectomy was performed under a combined intra- CEREBELLAR NUCLEI AND CONNECTIONS 171 venous pentothal and open drop ether anesthesia. The dura was nor- mal in appearance m was the postterior inferior surface of the left cerebellar hemisphere. At the junction of the tonsillar lobe with the biventral lobule, 2 cm lateral to the midline, a fine insulated needle was inserted in the direction of the dorsal portion of the left dentate nucleus. Three milliamperes of cautery current were passed through the needle for 45 seconds before it was removed. The cerebellum remained normal in appearance and continued to pulsate; there was no gross evidence of hemorrhage. The postoperative recovery was uneventful. Postoperatively the monkey sat in a normal position; the head remained upright without tilting abnormally to either side. The extraocular muscles appeared to function well and voluntary con- jugate movements of the eyes in all directions of gaze remained normal. Neither nystagmus nor nystagmoid movements developed. Although the monkey seemed reluctant to walk, run and jump for the first 24 hours she did so thereafter in a normal fashion. There was no evidence of ataxia or dysequilibrium in her gait. She was observed many times using both hands when eating or scratching. Except for clumsiness of the left hand for the first postoperative day no abnormalities such as tremor,
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