Innervation of monkey extraocular muscles: Localization of sensory and motor neurons by retrograde transport of horseradish peroxidase

Neurons that provide sensory and motor innervation of extraocular muscles in the monkey have been identified and localized by retrograde transport of horseradish peroxidase (HRP). Injections of HRP into individual extraocular muscles of rhesus or pig‐tail monkeys labeled pseudounipolar neurons that were localized within the ipsilateral semilunar ganglion. The distribution of labeled neurons within the ganglion was consistent with its somatotopic organization as the majority were found within the ophthalmic subdivision. Absence of labeled neurons within either the trigeminal mesencephalic or spinal nucleus was in agreement with previous findings in the cat (Porter and Spencer, '82). Intracranial transection of the ophthalmic nerve prior to muscle injection eliminated all labeling within the ganglion. These data indicate that the extraocular muscles can be selectively deafferented in order to examine the potential role(s) of proprioception in the neural control of eye movements.

[1]  K. B. Corbin Observations on the peripheral distribution of fibers arising in the mesencephalic nucleus of the fifth cranial nerve , 1940 .

[2]  B. Cohen,et al.  Eye muscle motor neurons with different functional characteristics. , 1972, Brain research.

[3]  P. Buisseret,et al.  Trigeminal pathway of the extrinsic eye muscle afferents in cat , 1975, Brain Research.

[4]  E. Manni,et al.  Extraocular muscle proprioception and the descending trigeminal nucleus. , 1971, Experimental neurology.

[5]  K. Maekawa,et al.  Activity of flocculus Purkinje cells during passive eye movements. , 1981, Journal of neurophysiology.

[6]  A. Graybiel,et al.  Some afferent connections of the oculomotor complex in the cat: an experimental study with tracer techniques. , 1974, Brain research.

[7]  C. Rovainen,et al.  Retrograde HRP labelling of the oculomotoneurons in adult lampreys , 1978, Brain Research.

[8]  R. Llinás,et al.  Mossy and climbing fiber projections of extraocular muscle afferents to the cerebellum. , 1972, Brain research.

[9]  J. D. Porter,et al.  Innervation and structure of extraocular muscles in the monkey in comparison to those of the cat , 1981, The Journal of comparative neurology.

[10]  J. D. Porter,et al.  Localization and morphology of cat extraocular muscle afferent neurones identified by retrograde transport of horseradish peroxidase , 1982 .

[11]  M. Lucchi,et al.  Afferent fibers and sensory ganglion cells within the oculomotor nerve in some mammals and man. I. Anatomical investigations. , 1977, Archives italiennes de biologie.

[12]  M. Glicksman,et al.  Localization of motoneurons controlling the extraocular muscles of the rat , 1980, Brain Research.

[13]  K. Akert,et al.  A TRANSSYNAPTIC AUTORADIOGRAPHIC STUDY OF THE PATHWAYS CONTROLLING THE EXTRAOCULAR EYE MUSCLES, USING [125I]B‐IIb TETANUS TOXIN FRAGMENT * , 1981, Annals of the New York Academy of Sciences.

[14]  E. Manni,et al.  Eye muscle proprioception and the semilunar ganglion. , 1966, Experimental neurology.

[15]  K. B. Corbin,et al.  FUNCTION OF MESENCEPHALIC ROOT OF FIFTH CRANIAL NERVE , 1940 .

[16]  R. Baker,et al.  Excitatory termination of abducens internuclear neurons on medial rectus motoneurons: relationship to syndrome of internuclear ophthalmoplegia. , 1978, Journal of neurophysiology.

[17]  R. Jampel,et al.  Muscle spindles in the extraocular muscles of the macaque. , 1966, The Journal of comparative neurology.

[18]  L E Mays,et al.  Neural control of vergence eye movements: activity of abducens and oculomotor neurons. , 1984, Journal of neurophysiology.

[19]  J. R. Augustine,et al.  Functional organization of the oculomotor nucleus in the baboon. , 1981, The American journal of anatomy.

[20]  R. Carpenter,et al.  Movements of the Eyes , 1978 .

[21]  L. Maffei,et al.  Instability of the eye in the dark and proprioception , 1977, Nature.

[22]  G. Lennerstrand,et al.  Motor unit responses in the lateral rectus muscle of the cat: intracellular current injection of abducens nucleus neurons. , 1976, Acta physiologica Scandinavica.

[23]  H. Barbas,et al.  Frontal projections of dorsal neck and extraocular muscles , 1977, Experimental Neurology.

[24]  G L Ruskell,et al.  The fine structure of innervated myotendinous cylinders in extraocular muscles of rhesus monkeys , 1978, Journal of neurocytology.

[25]  P. Luiten,et al.  Extraocular muscle representation in the brainstem of the carp , 1978, The Journal of comparative neurology.

[26]  A. Fuchs,et al.  Responses of fibers in medial longitudinal fasciculus (MLF) of alert monkeys during horizontal and vertical conjugate eye movements evoked by vestibular or visual stimuli. , 1976, Journal of neurophysiology.

[27]  E. Eldred,et al.  The occurrence of muscle spindles in extraocular muscles of various vertebrates , 1974, Journal of morphology.

[28]  C. Sherrington OBSERVATIONS ON THE SENSUAL RÔLE OF THE PROPRIOCEPTIVE NERVE-SUPPLY OF THE EXTRINSIC OCULAR MUSCLES , 1918 .

[29]  Y. Akagi The localization of the motor neurons innervating the extraocular muscles in the oculomotor nuclei of the cat and rabbit, using horseradish peroxidase , 1978, The Journal of comparative neurology.

[30]  R. Burde,et al.  Central origin of oculomotor parasympathetic neurons in the monkey , 1980, Brain Research.

[31]  D. Robinson,et al.  Oculomotor signals in medial longitudinal fasciculus of the monkey. , 1978, Journal of neurophysiology.

[32]  V. E. Pettorossi,et al.  Trigeminal afferent fibers in the trunk of the oculomotor nerve of lambs , 1976, Experimental Neurology.

[33]  J. Büttner-Ennever,et al.  Oculomotor nucleus afferents in the monkey demonstrated with horseradish peroxidase , 1979, Brain Research.

[34]  M. Carpenter,et al.  Abducens internuclear neurons and their role in conjugate horizontal gaze , 1980, The Journal of comparative neurology.

[35]  R. Baker,et al.  Physiological identification of interneurons and motoneurons in the abducens nucleus , 1975, Brain Research.

[36]  V C Abrahams,et al.  Projections of extraocular, neck muscle, and retinal afferents to superior colliculus in the cat: their connections to cells of origin of tectospinal tract. , 1975, Journal of neurophysiology.

[37]  M. Fillenz,et al.  Responses in the brainstem of the cat to stretch of extrinsic ocular muscles , 1955, The Journal of physiology.

[38]  D. Whitteridge,et al.  Nerve impulses in the brainstem of the goat. Short latency responses obtained by stretching the extrinsic eye muscles and the jaw muscles , 1953, The Journal of physiology.

[39]  W. Willis,et al.  The organization of the electromotor nucleus and extraocular motor nuclei in the stargazer (Astroscopus y‐graecum) , 1979, The Journal of comparative neurology.

[40]  R. Baker,et al.  Localization and morphology of cat retractor bulbi motoneurons. , 1980, Journal of neurophysiology.

[41]  P Bach-y-Rita,et al.  Conduction velocities in the abducens nerve correlated with vestibular nystagmus in cats. , 1968, Experimental neurology.

[42]  A. Fuchs,et al.  Extraocular muscle afferents to the cerebellum of the cat , 1969, The Journal of physiology.

[43]  D. Robinson,et al.  Absence of a stretch reflex in extraocular muscles of the monkey. , 1971, Journal of neurophysiology.

[44]  W. F. Allen Localization in the ganglion semilunare of the cat , 1924 .

[45]  A. A. Pearson The trochlear nerve in human fetuses , 1943 .

[46]  R. Warwick Representation of the extra‐ocular muscles in the oculomotor nuclei of the monkey , 1953, The Journal of comparative neurology.

[47]  I. Donaldson,et al.  Interactions between extraocular proprioceptive and visual signals in the superior colliculus of the cat. , 1980, The Journal of physiology.

[48]  P. Sterling,et al.  An electron microscope study of motoneurones and interneurones in the cat abducens nucleus identified by retrograde intraaxonal transport of horseradish peroxidase , 1977, The Journal of comparative neurology.

[49]  M. Correia,et al.  Medullary proprioceptive neurons from extraocular muscles in the pigeon identified with horseradish peroxidase , 1982, Brain Research.

[50]  G. Ruskell The incidence and variety of Golgi tendon organs in extraocular muscles of the rhesus monkey , 1979, Journal of neurocytology.

[51]  E. Manni,et al.  On whether eye muscle spindles are innervated by ganglion cells located along the oculomotor nerves. , 1970, Experimental neurology.

[52]  R. Baker,et al.  Morphophysiological identification of interneurons in the oculomotor nucleus that project to the abducens nucleus in the cat , 1975, Brain Research.

[53]  K. Akert,et al.  Medial rectus subgroups of the oculomotor nucleus and their abducens internuclear input in the monkey , 1981, The Journal of comparative neurology.