is there any sense in the palisade endings of eye muscles?

Ann. N.Y. Acad. Sci. ISSN 0077-8923

ANNALS OF THE NEW YORK ACADEMY OF SCIENCESIssue: Basic and Clinical Ocular Motor and Vestibular Research

Is there any sense in the Palisade endings of eye muscles?

Karoline Lienbacher,1 Michael Mustari,2 Bernhard Hess,3 Jean Buttner-Ennever,1

and Anja K.E. Horn1

1Institute of Anatomy I, Ludwig-Maximilians University of Munich, Germany. 2Washington National Primate Research Center,University of Washington, Seattle, Washington. 3Department of Neurology, University Hospital Zurich, Switzerland

Address for correspondence: Karoline Lienbacher, Institute of Anatomy I, LMU Munich, Pettenkoferstrasse 11, D-80336Munich, Germany. [email protected]

Palisade endings (PEs), which are unique to the eye muscles, are associated with multiply innervated muscle fibers.They lie at the myotendinous junctions and form a cap around the muscle fiber tip. They are found in all animalsinvestigated so far, but their function is not known. Recently, we demonstrated that cell bodies of PEs and tendonorgans lie around the periphery of the oculomotor nucleus in the C- and S-groups. A morphological analysis of theseperipheral neurons revealed the existence of different populations within the C-group. We propose that a small groupof round or spindle-shaped cells gives rise to PEs, and another group of multipolar neurons provide the multiplemotor endings. If PEs have a sensory function, then their cell body location close to motor neurons would be in anideal location to control tension in extraocular muscles; in the case of the C-group, its proximity to the preganglionicneurons of the Edinger–Westphal nucleus would permit its participation in the near response. Despite their unusualproperties, PEs may have a sensory function.

Keywords: oculomotor nucleus; C-group

Preferred citation: Lienbacher, K., M. Mustari, B. Hess, J. Buttner-Ennever & A.K.E. Horn. 2011. Is there any sense in the

Palisade endings of eye muscles? In Basic and Clinical Ocular Motor and Vestibular Research. Janet Rucker & David S. Zee,

Eds. Ann. N.Y. Acad. Sci. 1233: 1–7.

Introduction

The classical proprioceptors of skeletal muscle aremuscle spindles to measure length, and Golgi ten-don organs to measure force. Extraocular muscles(EOM) are a well-known exception to this, perhapsbecause they are characterized by embryological fea-tures, like immature skeletal muscles. They exhibita wide variation in sensory receptors dependingon species.1,2 The eye muscles of some vertebratespecies such as monkeys have few tendon organs(no classical Golgi tendon organs and no musclespindles);3 other species (e.g., human) have somemuscle spindles that appear underdeveloped and allof them with striking anomalies compared to sheepspindles.4 In contrast, artiodactyls (e.g., sheep, goat,camel) have well-developed tendon organs andmuscle spindles. But even in species without classicalproprioceptors, such as monkeys, representations ofeye position in the primary somatosensory cortex

have been demonstrated.5 Furthermore, a stretchreflex in the EOMs of different species with sparse,diminutive, or even absent muscle spindles has beenreported.6 The question considered in this article is,Which structure could provide this central proprio-ceptive information? One possibility is the palisadeendings.

Palisade endings (PEs) are unique to eye musclesand have been found in all species investigated sofar.4,7–12 Up to now PEs were assumed to be sen-sory on account of the location in the tendon8 andtheir similarity to immature Golgi tendon organs.13

However, recent studies have shown that they havesome properties typical of motor terminals: they arecholinergic and a small portion of PE terminals (ap-proximately 10%) are positive for �-bungarotoxin atthe postsynaptic site.14,15 Furthermore, Lienbacheret al.16 and Zimmermann et al.17 have shown thatPEs can be anterogradely filled by central tracerinjections into the region of the oculomotor or

doi: 10.1111/j.1749-6632.2011.06169.xAnn. N.Y. Acad. Sci. 1233 (2011) 1–7 c© 2011 New York Academy of Sciences. 1

Palisade endings of eye muscles Lienbacher et al.

abducens nucleus, respectively. In spite of these re-sults, in this paper we will present evidence support-ing the sensory function of PEs.

Tracer injections into the eye muscles of monkeyretrogradely label sensory ganglion cells and mo-tor neurons. The sensory pseudo-unipolar ganglioncells lie in the ophthalmic division of the trigeminalganglion;18,19 but different populations of neuronswere found both within and around the oculomo-tor, abducens, and trochlear nuclei. The neuronswithin the boundaries of the classical motor nu-clei were shown to innervate the singly-innervatedfibers, whereas the peripheral cell groups were as-sumed to innervate the multiply-innervated musclefibers and possibly PEs. The peripheral cell groupsfor medial rectus and inferior rectus comprise theC-group and those for inferior oblique and superiorrectus the S-group.20 In this study, we have analyzedthe peripheral cell group of the medial rectus ofmonkeys (C-group) in more detail with focus onsize and morphology of neurons. A few neuronsshowed a morphology resembling that of trigemi-nal ganglion cells and may represent the cell bodiesof sensory PEs.

Methods

All experimental procedures conformed to the stateand university regulations for laboratory animalcare, including the Principles of Laboratory AnimalCare (NIH Publication 85-23, revised 1985), andthey were approved by animal care officers and theInstitutional Animal Care and Use Committees andwere described in detail in a previous report.20

Macaque monkeys were injected in the belly orthe distal tip of the medial rectus muscle with choler-atoxin subunit B (CTB) or wheat-germ-agglutininhorseradish peroxidase (WGA-HRP). After a sur-vival time of three days, the animals were killed andtranscardially perfused as described previously.20

The brainstem and the orbits were removed andcut transversely at 20 �m (eye muscles) and 40 �m(brainstem).

For the immunocytochemical detection of CTB,free-floating brain sections were pretreated with10% methanol and 3% H2O2 to suppress endoge-nous peroxidase activity and were then preincubatedin 0.1M phosphate buffer (PB) at pH 7.4 containing0.3% Triton X-100 with 5% normal rabbit serumfor 1 h. Then, the tissue was processed with goatanti-CTB (1:40,000; List Biological Laboratories,

CA) for 48 h at 4◦ C. The sections were washed in0.1M PB three times and treated with biotinylatedrabbit anti-goat (1:200; Vector Labs, Burlingame,CA) for 1 h at room temperature. Then the sec-tions were washed in 0.1M PB three times and incu-bated in avidin–biotin complex (1:50; Vector Labs,Burlingame, CA) for one hour at room temperature.After two rinses in 0.1M PB and one rinse in 0.05MTris buffer solution (TBS, pH 8.0), the antigenicsites were visualized with 0.05% diaminobenzidine(DAB) and 0.01% H2O2 in 0.05 M TBS (pH 8.0)for 5–10 minutes. The sections were mounted, air-dried, dehydrated, and cover-slipped in Depex. TheWGA-HRP was visualized with the tetramethylben-zidine method as described previously.20

Seven macaque monkeys with tracer injections(CTB or WGA) into the MR, and one additionalmacaque monkey with a tracer injection (CTB) intothe distal part of the superior rectus muscle (SR)were carefully reanalyzed. The focus lay on the ex-amination of the peripheral C-group neurons of theMR. We distinguished between C-group neuronsin close proximity to the dorsomedial aspect of theoculomotor nucleus (nIII) (after belly injections)and those which extend far rostral to nIII encirclingthe preganglionic neurons of the Edinger–Westphalnucleus (EWpg; after distal injections into themyotendinous junction).

The sections of a supplementary case containingnIII and immunostained for the cholinergic markercholine acetyltransferase (ChAT) were analyzed forthe morphology of the peripheral neurons in the C-group. The cholinergic C-group neurons can be dis-tinguished from preganglionic neurons of the EWpg

as another cholinergic neuron group in the peri-oculomotor region by their different histochemicalproperties, for example, lack of non-phosphorylatedneurofilaments and cytochrome oxidase.21,22

The slides were examined with a Leica micro-scope (DMRB; Leica, Bensheim, Germany) underbright field conditions. Micrographs were takenwith a digital camera (Pixera Pro 600 ES; Klugham-mer, Markt Indersdorf, Germany), captured on acomputer (Pixera Viewfinder software; Klugham-mer), and processed with image analysis software(Photoshop 11.0; Adobe Systems, Mountain View,CA). The images were arranged and labeled usingdrawing software (CorelDraw 11.0; Corel, Ottawa,Ontario, Canada). A morphometric analysis wasperformed on digitized images taken at a

2 Ann. N.Y. Acad. Sci. 1233 (2011) 1–7 c© 2011 New York Academy of Sciences.

Lienbacher et al. Palisade endings of eye muscles

40× magnification. Only those cells with a clearlyvisible nucleus were measured with ImageJ software.The mean diameter in micrometer was calculated inExcel 2007 by [Dmin + Dmax]/2.

Results

Morphological and morphometric analysis of thenIII peripheral groups revealed a heterogeneous cellpopulation. Belly tracer injections into the MR ledto retrogradely labeled twitch motor neurons withinnIII and neurons in the periphery of nIII, with thelargest accumulation within the C-group adjacentto the dorsomedial aspect of nIII. Very distal tracerinjections into the myotendinous junction, mostlysparing muscle fibers, resulted in exclusive labelingof the peripheral neurons around nIII, some of themextending dorsally to nIII encircling the EWpg

23 andalso far rostrally to nIII.

After a systematic inspection of the peripheraleither tracer-labeled or ChAT-labeled neurons, wefound numerous multipolar neurons—a morphol-ogy typical for motor neurons (Fig. 1B). We alsoidentified a small but consistent population of neu-rons that were round or bipolar—a morphology(Fig. 1A) resembling the sensory ganglion cells of themesencephalic trigeminal nucleus (V mes; Fig. 1C).The population lay closer to the EWpg, and distantfrom nIII; and, importantly, they were only back-labeled after very distal tracer injections. These twodifferent morphological cell types were also seen intracer labeled neurons of the S-group after a tracerinjection into the myotendinous junction of the SR(Fig. 1D).

The morphometric analysis of the peripheraltracer-labeled neurons around nIII revealed a two-peak cell size profile (Fig. 2): (1) tracer-positive pre-sumed twitch motor neurons within nIII after bellyinjections into the MR had a large mean diame-ter (22–34 �m), whereas (2) the mean diameterof tracer-labeled peripheral C-group neurons afterbelly injections ranged across a large cell size spec-trum with addition small cells (14–38 �m). A pop-ulation of smaller neurons (3) was seen within thetracer-labeled neurons far rostral to nIII after distalinjections into the myotendinous junction of MR(14–22 �m).

Discussion

The eye muscles consist of two separate fibertypes: the singly innervated (SIF) twitch musclefibers in the global layer innervated by single en

Figure 1. (A, B) The immunoperoxidase staining for cholineacetyltransferase (ChAT) of peripheral C-group neurons in themonkey. (C) Ganglion cells within the mesencephalic trigeminalnucleus immunostained for nonphosphorylated neurofilament(NP-NF). Note the similarity to the peripheral C-group neuronin A. (D) Retrograde tracer-labeled (WGA-HRP) spindle-shaped(closed arrow) and multipolar (open arrow) neuron in the S-group after a distal tracer injection into the superior rectusmuscle of a monkey.

plaque terminals and the multiply innervated (MIF)non-twitch muscle fibers innervated by multipleen grappe terminals along the whole muscle length.The MIFs of the orbital layer are additionally inner-vated by en plaque endings at their central part.24

The PEs represent special nerve endings unique to

Ann. N.Y. Acad. Sci. 1233 (2011) 1–7 c© 2011 New York Academy of Sciences. 3


Figure 2. Cell size profile of internal and peripheral neurons of nIII. Histogram demonstrating the cell size profile of labeledneurons after tracer injections into the distal or central part of the medial rectus muscle (MR). Note that no major differences ofthe cell size profile of peripheral and central neurons are present after belly injection. However, small-sized cells in the peripheralcell groups are only present after tracer injections into the distal muscle (myotendinous junction).

eye muscles, which are exclusively associated withMIFs at the myotendinous junctions of the mus-cle. PEs are found in all animals being investigatedso far, and recently their cell bodies were shownto be located in or around the motor nuclei ofEOMs.16,17 It is still not clear what function thePEs have and whether they are motor14 or sen-sory25 organs. Recent findings, such as the asso-ciation with cholinergic markers,14 and the fact thatthey could be tracer labeled from central tracer in-jections in or around the motor nuclei,16,17 sug-gest a motor function of these endings. Otherwise,the location of PEs at the myotendinous junctionsand their continuity with tendon endings indi-cate a sensory function,16 putting the assumptionof a pure motor function into question.

Tracer injections into primate eye musclesshowed that the motor neurons of the en plaqueendings innervating the SIFs lay within the motornuclei and the cell bodies of the en grappe endingsinnervating the MIFs are located in the periphery ofthe motor nuclei.20 Distal tracer injections into theeye muscle showed only the MIF neurons, whereasbelly injections showed the SIF and the MIF neu-rons.20 Until now the peripheral neurons aroundthe motor nucleus have generally been consideredas MIF neurons forming one population of neu-rons whose neuromuscular multiple nerve endingsare distributed along the whole muscle fiber lengthreaching up to the distal and proximal ends of theeye muscle. However, these distal tracer injections

also involve the PEs and tendon organs at the my-otendinous junctions and in the tendon. In lightof our recent findings that the cell bodies of PEsare located in the periphery of the motor nuclei,the peripheral cell groups, back-labeled after tracerinjections into the myotendinous junction, it mustbe considered that some are back-labeled also fromPEs. Theoretically, there are two possibilities of orga-nization as already suggested previously:20 either theperipheral neurons around the motor nuclei formone homogenous population of neurons that giverise to multiple en grappe endings and PEs plus ten-don organs, or there are at least two different neuronpopulations, for example, cell bodies of the motoren grappe endings and cell bodies of possible sensoryPEs.

Our analysis of the peripheral neurons aroundnIII revealed two groups of neurons based on cellsize but also morphological differences (Fig. 1).The findings of this reanalysis are in good accor-dance with previous data on the cell sizes com-paring tracer-labeled peripheral and tracer-labeledpresumed twitch-neurons within nIII after a largetracer injection into the muscle belly, where a bi-modal distribution of cell sizes was noted, as well(Buttner-Ennever et al., see Fig. 13A20). As in theprevious paper, no difference in cell sizes of retro-gradely labeled neurons in the peripheral and cen-tral, presumed twitch-motoneurons, were noted af-ter a tracer injection in the belly (Buttner-Enneveret al.,20 see Fig. 2). We extended this morphometric



Figure 3. The oculomotor nuclei (III) with their peripheral cell groups. (A) The oculomotor nucleus containing the motor neuronsof the medial rectus (MR) with A- and B-groups, inferior rectus (IR), inferior oblique (IO), and superior rectus (SR) muscle. ThenIII has different peripheral groups: the C containing neurons of IR and MR—and S-group containing neurons of SR and IO. (B)The peripheral neurons of the superior oblique muscle form a cap dorsal to the trochlear nucleus (IV). (C) The peripheral neuronsof the lateral rectus muscle are located around the medial and dorsal aspect of the abducens nucleus (VI).

analysis by comparing the cell sizes of peripheral cellgroups around the EWpg and those of peripheralcells adjacent to nIII only back-labeled after distaltracer injections and found a bimodal distribution,with the latter group being the larger cells.

Only tracer injections into the myotendinousjunction—the location of PEs—revealed, in addi-tion, a group of round or spindle-shaped neu-rons with a morphology resembling that of sen-sory ganglion cells26 (Fig. 1). A similar attempt of



classification based on morphological cell fea-tures of tracer-labeled neurons after EOMinjections was undertaken in the pig.27 Multipo-lar large cells were considered as alpha motoneu-rons corresponding to twitch motoneurons andsmall cells as �-motoneurons, which may repre-sent the non-twitch motoneurons providing multi-ple innervation and their spindle-shaped and roundneurons—suggested as sensory cell bodies of spin-dle afferents—may represent the cell bodies of PEs.Although the possibility of the location of sensoryneuronal cell bodies so close to the motor nuclei(Fig. 3), and not in a separate ganglion, does notseem obvious, there is at least one example of well-known sensory neurons in the brainstem. The largeround ganglion-like neurons of the mesencephalictrigeminal nucleus (V mes) located close to the fourthventricle at pontine levels and as single neuronsat the border of the periaqueductal gray at mes-encephalic levels represent well-described sensoryneurons innervating the muscle spindles of the jawmuscles.26,28 Furthermore, several studies indicatethat at least part of them may innervate musclespindle afferents of the eye muscles.29,30 Becausewe never saw tracer labeled V mes cells after distalinjections of the EOM,16 this nucleus was ruled outas a source of PEs. In addition, tracer injectionsinto the medullary part of V mes did not result inanterogradely labeled PEs.17

Based on the findings that only tracer injectionsinto the myotendinous junction of MR revealedtwo populations of peripheral neurons—differingin their cell sizes and/or morphology—we proposethat the round neurons within the peripheral cellgroups represent sensory cell bodies of the PEs.These sensory cells in the periphery of nIII are as-sumed to give rise to sensory terminals of PEs, andthe multipolar neurons in the periphery of nIII torepresent MIF motor neurons, innervating the non-twitch muscle fibers via multiple en grappe endings(Fig. 4). Only active MIFs would provide a tensionon the tendon thereby transferring the informa-tion to sensory palisade ending terminals. A cen-tral circuit between sensory and motor pathwayswould stimulate the MIF motor neurons therebymodulating the MIF activity.

In conclusion, our results show that the periph-eral cell groups (S- and C-group) of nIII con-tain separate populations of neurons with differentmorphology and with different cell size profile. We

Figure 4. Schematic drawing of the myotendinous junctionand its innervation illustrating a hypotheses for palisade ending(PE) function. Two functionally different sets of neurons withinthe peripheral MIF-motor neuron groups provide innervationof the myotendinous junction. Sensory neurons give rise to PEsand motor neurons provide multiple innervation by en grappeendings. A stretch of the myotendinous junction would transmita sensory signal via the PEs centrally to activate MIF-motorneurons.

suggest that one cell population of neurons witha multipolar shape represent the cell bodies of theen grappe motor terminals innervating non-twitchfibers, and the other group of round neurons closerto EWpg are likely to represent the cell bodies ofsensory palisade endings (Fig. 4). Further record-ing studies on the different populations in thenIII periphery, or selective small tracer-injectionsinto both groups, are necessary to prove thishypothesis.

Acknowledgments

This work was supported by Deutsche Forschungs-gemeinschaft DFG HO 1639/4-3 (K.L., J.B.,A.K.E.H.), National Institutes of Health EY020744;RR00166 (M.M.), Swiss National Science Founda-tion Grant 3100A0-110802, and the Betty and DavidKoetser Foundation for Brain Research (B.H.).

Conflicts of interest

The authors declare no conflicts of interest.

References

1. Cilimbaris, P.A. 1910. Histologische Untersuchungen uberdie Muskelspindeln der Augenmuskeln. Arch. mikro. Anat.und Entwicklungsgeschichte. 75: 692–747.

2. Harker, D.W. 1972. The structure and innervation of sheepsuperior rectus and levator palpebrae extraocular eye mus-cles. II: Muscle spindles. Invest. Ophthalmol. Vis. Sci. 11:970–979.



3. Maier, A., M. DeSantis & E. Eldred. 1974. The occurrenceof muscle spindles in extraocular muscles of various verte-brates. J. Morph. 143: 397–408.

4. Ruskell, G.L. 1999. Extraocular muscle proprioceptors andproprioception. Prog. Retin. Eye Res. 18: 269–291.

5. Wang, X., M. Zhang, I.S. Cohen & M.E. Goldberg. 2007.The proprioceptive representation of eye position in monkeyprimary somatosensory cortex. Nat. Neurosci. 10: 640–646.

6. Dancause, N., M.D. Taylor, E.J. Plautz, et al. 2007. A stretchreflex in extraocular muscles of species purportedly lackingmuscle spindles. Exp. Brain Res. 180: 15–21.

7. Dogiel, A.S. 1906. Die Endigungen der sensiblen Nerven inden Augenmuskeln und deren Sehnen beim Menschen undden Saugetieren. Arch. mikro. Anat . 68: 501–526.

8. Alvarado-Mallart, R.M. & M. Pincon Raymond. 1979. Thepalisade endings of cat extraocular muscles: a light and elec-tron microscope study. Tissue Cell. 11: 567–584.

9. Billig, I., C. Buisseret-Delmas & P. Buisseret. 1997. Identi-fication of nerve endings in cat extraocular muscles. Anat.Rec. 248: 566–575.

10. Ruskell, G.L. 1978. The fine structure of innervated my-otendinous cylinders in extraocular muscles in rhesus mon-key. J. Neurocytol. 7: 693–708.

11. Blumer, R., J.R. Lukas, R. Wasicky & R. Mayr. 1998.Presence and structure of innervated myotendinous cylin-ders in sheep extraocular muscle. Neurosci. Lett . 248: 49–52.

12. Eberhorn, A.C., A.K.E. Horn, N. Eberhorn, et al. 2005. Pal-isade endings in extraocular eye muscles revealed by SNAP-25 immunoreactivity. J. Anat. 205: 307–315.

13. Zelena, J. & T. Soukup. 1977. The development of Golgitendon organs. J. Neurocytol. 6: 171–194.

14. Konakci, K.Z., J. Streicher & W. Hoetzenecker. 2005. Pal-isade endings in extraocular muscles of the monkey areimmunoreactive for choline acetyltransferase and vesicularacetylcholine transporter. Invest. Ophthalmol. Vis. Sci. 46:4548–4554.

15. Blumer, R., K.Z. Konakci, C. Pomikal, et al. 2009. Palisadeendings: cholinergic sensory organs or effector organs? In-vest. Ophthalmol. Vis. Sci. 50: 1176–1186.

16. Lienbacher, K., M. Mustari, H.S. Ying, et al. 2011. Do pal-isade endings in extraocular muscles arise from neurons inthe motor nuclei? Invest. Ophthalmol. Vis. Sci. 52: 2510–2519.

17. Zimmermann, L., P.J. May, A.M. Pastor, et al. 2011. Evidencethat the extraocular motor nuclei innervate monkey palisadeendings. Neurosci. Lett . 489: 89–93.

18. Porter, J.D., B.L. Guthrie & D.L. Sparks. 1983. Innervationof monkey extraocular muscles: localization of sensory and

motor neurons by retrograde transport of horseradish per-oxidase. J. Comp. Neurol. 218: 208–219.

19. Fackelmann, K., A. Nouriani, A.K. Horn & J.A. Buttner-Ennever. 2008. Histochemical characterisation of trigeminalneurons that innervate monkey extraocular muscles. Prog.Brain Res. 171: 17–20.

20. Buttner-Ennever, J.A., A.K.E. Horn, H. Scherberger & P.D’Ascanio. 2001. Motoneurons of twitch and nontwitchextraocular muscle fibers in the abducens, trochlear, andoculomotor nuclei of monkeys. J. Comp. Neurol. 438:318–335.

21. Eberhorn, A.C., P. Ardelenanu, J.A. Buttner-Ennever &A.K.E. Horn. 2005. Histochemical differences between mo-toneurons supplying multiply and singly innervated extraoc-ular muscle fibers. J. Comp. Neurol. 491: 352–366.

22. Horn, A.K., A. Eberhorn, W. Hartig, et al. 2008. Periocu-lomotor cell groups in monkey and man defined by theirhistochemical and functional properties: reappraisal of theEdinger-Westphal nucleus. J. Com. Neurol. 507: 1317–1335.

23. Kozicz, T., J.C. Bittencourt, P.J. May, et al. 2011. The Edinger-Westphal nucleus: a historical, structural, and functionalperspective on a dichotomous terminology. J. Comp. Neurol.519: 1413–1434.

24. Spencer, R.F. & J.D. Porter. 2006. Biological organization ofthe extraocular muscles. Prog. Brain Res. 151: 43–80.

25. Buttner-Ennever, J.A., A.C. Eberhorn & A.K.E. Horn. 2003.Motor and sensory innervation of extraocular eye muscles.Ann. N.Y. Acad. Sci. 1004: 40–49.

26. Johnston, J.B. 1909. The radix mesencephalica trigemini.J. Comp. Neurol. 19: 593–644.

27. Kubota, K., S. Matsuyama, M. Kubota, et al. 1988. Local-ization of proprioceptive neurons innervating the musclespindles of pig extraocular muscles studied by horseradishperoxidase labelling. Anat. Anz. 166: 117–131.

28. Alvarado-Mallart, M.R., C. Batini, C. Buisseret-Delmas &J. Corvisier. 1975. Trigeminal representations of the mas-ticatory and extraocular proprioceptors as revealed byhorseradish peroxidase retrograde transport. Exp. Brain Res.23: 167–179.

29. Wang, N. & P.J. May. 2008. Peripheral muscle targets andcentral projections of the mesencephalic trigeminal nucleusin macaque monkeys. J. Comp. Neurol. 291: 974–987.

30. Bortolami, R., M.L. Lucchi, V.E. Pettorossi, et al. 1987. Lo-calisation and somatotopy of sensory cells innervating theextraocular muscles of lamb, pig and cat. Histochemicaland electrophysiological investigation. Arch. Ital. Biol. 125:1–15.


is there any sense in the palisade endings of eye muscles?

Documents