Twitch and Nontwitch Motoneuron Subgroups in the Oculomotor Nucleus of Monkeys Receive Different Afferent Projections
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THE JOURNAL OF COMPARATIVE NEUROLOGY 479:117–129 (2004)
Twitch and Nontwitch Motoneuron
Subgroups in the Oculomotor Nucleus of
Monkeys Receive Different Afferent
Projections
RICHARD WASICKY,1 ANJA K.E. HORN,2 AND JEAN A. BÜTTNER-ENNEVER2*
1
Institute of Anatomy, University of Vienna, 1090 Vienna, Austria
2
Institute of Anatomy, Ludwig-Maximilian University, 80336 Munich, Germany
ABSTRACT
Motoneurons in the primate oculomotor nucleus can be divided into two categories, those
supplying twitch muscle fibers and those supplying nontwitch muscle fibers. Recent studies
have shown that twitch motoneurons lie within the classical oculomotor nucleus (nIII), and
nontwitch motoneurons lie around the borders. Nontwitch motoneurons of medial and infe-
rior rectus are in the C group dorsomedial to nIII, whereas those of inferior oblique and
superior rectus lie near the midline are in the S group. In this anatomical study, afferents to
the twitch and nontwitch subgroups of nIII have been anterogradely labeled by injections of
tritiated leucine into three areas and compared. 1) Abducens nucleus injections gave rise to
silver grain deposits over all medial rectus subgroups, both twitch and nontwitch. 2) Later-
ally placed vestibular complex injections that included the central superior vestibular nu-
cleus labeled projections only in twitch motoneuron subgroups. However, injections into the
parvocellular medial vestibular nucleus (mvp), or Y group, resulted in labeled terminals over
both twitch and nontwitch motoneurons. 3) Pretectal injections that included the nucleus of
the optic tract (NOT), and the olivary pretectal nucleus (OLN), labeled terminals only over
nontwitch motoneurons, in the contralateral C group and in the S group. Our study demon-
strates that twitch and nontwitch motoneuron subgroups do not receive identical afferent
inputs. They can be controlled either in parallel, or independently, suggesting that they have
basically different functions. We propose that twitch motoneurons primarily drive eye move-
ments and nontwitch motoneurons the tonic muscle activity, as in gaze holding and vergence,
possibly involving a proprioceptive feedback system. J. Comp. Neurol. 479:117–129, 2004.
© 2004 Wiley-Liss, Inc.
Indexing terms: abducens nucleus; vestibuloocular pathways; pretectum; slow muscle fibers;
proprioception in eye muscle; vergence
The activity of extraocular motoneurons is tightly for muscle motor innervation. However, in mammals
linked to eye position in behaving monkeys. In some neu- there are at least six or seven different types of extraocu-
rons the tonic component of activity predominates, lar muscle fibers (Spencer and Porter, 1988). Recent stud-
whereas in others the phasic component does. In both ies have attempted to correlate the speed and fatigue-
groups, there is a wide spectrum of recruitment thresholds
(Fuchs et al., 1988; Dean, 1996). Nevertheless, all the
motoneurons recorded until now behave in the same way, Grant sponsor: German Research Council; Grant number: DFG HO
in that they participate in every type of eye movement, 1639/4-P.
independently of whether it is saccadic, vestibular, or *Correspondence to: Jean A. Büttner-Ennever, Inst. Anatomy, Ludwig-
vergence in nature (Keller and Robinson, 1972; Mays, Maximilian University Munich, Pettenkoferstr. 11, 80336 Munich, Ger-
many. E-mail: buettner@anat.med.uni-muenchen.de
1984), albeit with different sensitivities (Gamlin and Received 30 August 2002; Revised 24 March 2004; Accepted 24 June
Mays, 1992). Such results have led to the generally ac- 2004
cepted view that these motoneurons form a relatively ho- DOI 10.1002/cne.20296
mogeneous group, which provides the final common path Published online in Wiley InterScience (www.interscience.wiley.com).
© 2004 WILEY-LISS, INC.118 R. WASICKY ET AL.
based criteria of extraocular motor units with this six extraocular eye muscles in monkey. Twitch motoneu-
morphology (Shall et al., 1996), but it remains unclear rons reside within the boundaries of the classical motor
how each unit or muscle fiber type contributes to the wide nuclei, and the nontwitch motoneurons are found around
repertoire of eye movements seen in different species. The the periphery. In the abducens nucleus they form a cres-
unit and muscle fiber types can be divided into two main cent around the medial border, and in the trochlear nu-
categories, twitch fibers, which respond to electrical stim- cleus they form a dorsal cap. In the oculomotor nucleus
ulation with a fast twitch propagated throughout the fiber, (nIII) the nontwitch motoneurons of the medial and infe-
and nontwitch fibers, which respond to stimulation with a rior rectus (MR, IR) lie together in the C group (see Fig. 1),
slow tonic, nonpropagated, contraction (Lennerstrand, and those of the inferior oblique (IO) and superior rectus
1975; Bondi and Chiarandini, 1983). These two classes of (SR) lie on the midline, sandwiched between the two ocu-
muscle fiber are the original “Fibrillenstruktur and lomotor nuclei. Consequently, we have here chosen to call
Felderstruktur” fibers described by Siebeck and Kruger this midline IO/SR nontwitch motoneuron cluster the S
(1955) and the “singly and multiply innervated” extraoc- group.
ular muscle fibers of Mayr et al. (1975) and Spencer and Now that the anatomical location of at least some non-
Porter (1988). twitch motoneurons has been defined, we have begun to
Nontwitch muscle fibers occur more widely in reptilian study their afferent inputs, in an attempt to understand
and avian skeletal muscles, but in mammals they are their role in eye movements. We chose three premotor
found almost exclusively in extraocular eye muscles (Mor- regions, the abducens nucleus (nVI), the vestibular com-
gan and Proske, 1984). They have a much slower rise in plex, and the pretectum (PT), and used the tracer
tension to tetanic nerve stimulation than twitch fibers, are [3H]leucine to label afferent axonal terminals over the
very resistant to fatigue, and are suited to maintaining twitch motoneurons and nontwitch motoneurons of the
tension over long periods (Browne, 1976; Lennerstrand oculomotor nucleus. The results show that the twitch and
and Nichols, 1977; Morgan and Proske, 1984; Nelson et nontwitch subgroups do not have identical afferent inputs.
al., 1986). On the basis of these properties, the nontwitch For example, pretectal afferents target the nontwitch mo-
muscle fibers would be suited to a tonic function in eye toneurons, and some parts of the vestibular complex
muscle control. Physiological evidence to support this project to both types of motoneurons, whereas other ves-
comes from recordings of abducens units innervating slow tibular regions innervate only twitch motoneurons. This
tonic (i.e., nontwitch) muscle fibers in the cat (Goldberg et forms the foundation of the hypothesis that the two mo-
al., 1981) and in the frog (Dieringer and Precht, 1986). toneuron types play different roles in eye movement con-
However no recordings have been made from identified trol.
nontwitch motoneurons in behaving mammals, so it re-
mains unclear what their function is. Furthermore, how
the nontwitch muscle fibers contribute to different types of MATERIALS AND METHODS
eye movements, such as saccades, vestibuloocular reflex, All experimental procedures conformed to the State and
vergence, or smooth pursuit, remains to be determined. University regulations on Laboratory Animal Care, in-
Twitch fibers are innervated by a single central motor cluding the Principles of Laboratory Animal Care (NIH
endplate zone, whereas the slower nontwitch fibers are publication 85-23, revised 1985), and they were approved
multiply innervated along the whole of their length. Mak- by the Animal Care Officers and Institutional Animal
ing use of this difference in innervation patterns, Büttner- Care and Use Committees.
Ennever et al. (2001) retrogradely labeled only the non-
twitch motoneurons by making tracer injections into the Anterograde transport of [3H]leucine
distal tip of the eye muscles, thus avoiding the central Macaque monkeys received [3H]leucine injections into
endplate zone. The nontwitch motoneurons were found to one of three regions: the abducens nucleus (Z8, Macaca
lie separately from the “fast, twitch” motoneurons for all mulatta; Z21, M. mulatta), the vestibular complex (H19,
Abbreviations
A A group of MR motoneurons mvm magnocellular medial vestibular nucleus
aPT anterior pretectal nucleus mvp parvocellular medial vestibular nucleus
ATD ascending tract of Deiters nIII oculomotor nucleus
B B group of MR motoneurons nVI abducens nucleus
BC brachium conjunctivum nVII facial nucleus
C C group, MR and IR nontwitch motoneurons NOT nucleus of the optic tract
CCN central caudal nucleus nPC nucleus of the posterior commissure
d dentate nucleus OLN olivary pretectal nucleus
EW Edinger-Westphal
PC posterior commissure
iC interstitial nucleus of Cajal
pph nucleus prepositus hypoglossi
IO inferior oblique muscle
Pu pulvinar
io inferior olive
IR inferior rectus muscle S S group, IO and SR nontwitch motoneurons
Li nucleus limitans soa supraoculomotor area
lvc lateral visceral cell column of EW complex SR superior rectus muscle
lv lateral vestibular nucleus sv superior vestibular nucleus
MLF medial longitudinal fasciculus TMB tetramethyl benzidine
MR medial rectus muscle WGA-HRP wheat germ agglutinin-horseradish peroxidase
mv medial vestibular nucleus Y Y group of the vestibular complexOCULOMOTOR AFFERENTS TO NONTWITCH MOTONEURONS 119
M. mulatta; Z30, M. artiodes; A4-90, M. mulatta), and the of the medial rectus muscle (MR) was targeted and in the
pretectum (C9211, M. fascicularis; C9004, M. fascicularis; second case (B55, M. fascicularis) the distal part of infe-
A1189, M. mulatta). With animals under general anesthe- rior oblique (IO). Nontoxic cholera toxin subunit B (CT)
sia and under aseptic conditions, a small hole was tre- was also injected into the inferior rectus (IR) in one of
phined in the skull according to the coordinates of an atlas these cases (B55; 5 !l, 1%; List, Campbell, CA), and finally
(Snider and Lee, 1961; Shanta et al., 1968). In all exper- CT was deposited into the superior rectus (SR) in a third
iments [3H]leucine was concentrated to 80 –100 !Ci/!l, monkey (ZU, M. mulatta). After 2–3 days of survival, the
and 0.2–1.0 !l was injected by pressure through a glass animals received an overdose of Nembutal and were tran-
micropipette. In three cases, the injection site was local- scardially perfused with 4% paraformaldehyde in 0.1 M
ized from the coordinates in the atlas (Z8, Z30, and Z21). phosphate-buffered saline (PBS). The brain was trans-
In the other five cases, the oculomotor/trochlear nucleus ferred to sucrose solutions (10 –30% PBS) for frozen sec-
border was defined with microstimulation (3–10 !A), by tioning. To visualize the WGA-HRP, the sections (50 !m)
using insulated tungsten electrodes with the tip exposed were processed with the TMB method (Horn and Hoff-
for approximately 50 !m. Tracks were run until reproduc- mann, 1987). Cholera toxin was detected by immunohis-
ible, fast eye movements were evoked, in the appropriate tochemical methods on a separate series of sections
directions for the activation of superior oblique motoneu- (Büttner-Ennever et al., 2001).
rons. From these coordinates the injection site was calcu-
lated according to the atlas. The stimulation electrode was Data analysis of cell sizes
then withdrawn, and the injection micropipette was intro- The somatic areas of labeled neurons were estimated
duced at the appropriate location. with an image analysis system (Optimas) and a 3-CCD
After a survival time of 2–3 weeks, the animals were video camera mounted on a microscope. All the injection
killed with an overdose of Nembutal (80 mg/kg body sites are displayed here as right-side injections, to facili-
weight) and transcardially perfused with 0.9% saline tate the analysis. Images of brightfield photographs were
(35°C), followed by 2% paraformaldehyde with 1% glutar- digitalized by using a 3-CCD video camera mounted on a
aldehyde in 0.1 M phosphate buffer solution (pH 7.4). The microscope. The images were captured with Adobe Photo-
brains were immersed in 10% sucrose in 0.1 M phosphate shop 4.0. After conversion into black and white, the sharp-
buffer and transferred to 30% sucrose for 4 days. Blocks ness, contrast, and brightness were adjusted to reflect the
from these brains were cut at 40 !m on a freezing mic- appearance of the labeling seen through the microscope.
rotome in the frontal or, rather, the stereotaxic plane, i.e., Darkfield images were photographed on a Nikon Biophot
the same plane as in the atlas. The sections were mounted microscope. The photographs were digitalized by scanning
on gelatinized slides, cleared, rehydrated, and dried in an and then adjusted as described above.
oven for 48 hours at 40°C. In the darkroom, the slides
were dipped in Kodak NTB-3 or NTB-2 nuclear track
emulsion diluted 1:1 with distilled water and dried for 4 RESULTS
hours. After exposure for 4 or 8 weeks at 4°C, depending
on the emulsion used, the slides were developed in Kodak
Nontwitch motoneuron subgroups in the
D-19 developer for 4 minutes at 12–15°C and fixed in oculomotor nucleus
Tetanal superfix (diluted 1:9 in distilled water) for 10 To demonstrate the location of the nontwitch motoneu-
minutes. After being washed for 2 hours in running water, rons in the oculomotor nucleus, a large injection of WGA-
the sections were counterstained with cresyl violet, dehy- HRP (B61) was made into the belly of the medial rectus
drated, and coverslipped with Depex. The sections were muscle. Three distinct groups of motoneurons are retro-
examined, drawn, and photographed with a light micro- gradely labeled, the A and B group containing twitch
scope under darkfield and brightfield illumination. motoneurons and the C group containing nontwitch mo-
toneurons according to Büttner-Ennever et al. (2001; see
Tracer selectivity and sensitivity Fig. 1A). In agreement with other studies, we found that
In this study, we confined our observations to experi- the A and B group motoneurons were nearly the same
ments using the tracer tritiated leucine, as visualized via size, but the C group neurons were significantly smaller (A
autoradiography. The major advantage of this technique motoneurons: 356.3 " 94 !m2 mean area " SD, n # 58; B
is that [3H]leucine is taken up only by somata and not by motoneurons: 386.7 " 118.7 !m2, n # 54; C group: 221.5 "
axons. Therefore, unlike the case in most tract tracers, 58 !m2, n # 57; P # 0.001, SPSS 7.5 two-tailed Student’s
there is no spurious labeling resulting from uptake of the t-test; Büttner-Ennever and Akert, 1981; McClung et al.,
tracer by fibers, for example, by fibers of passage at the 2001).
injection site (Künzle, 1989). However, one disadvantage An injection of CT made into the distal tip of IR mainly
of autoradiography is that it is not as sensitive as some avoided the central endplate zone. It labeled many non-
detection methods using immunological or histochemical twitch motoneurons in the C group (Fig. 1B). A few large
techniques, so weak projections may remain undetected. twitch motoneurons in the classical IR subgroup were also
Unlike proline, leucine is not transported transysnapti- filled with CT (Fig. 1B, arrow). The twitch and nontwitch
cally. motoneurons of IR lie adjacent to each other, so, when
both are retrogradely filled, the IR nontwitch motoneu-
Wheat germ agglutinin-horseradish rons in the C group do not stand out clearly as they do in
peroxidase labeling the MR.
In two additional monkeys a solution of wheat germ An injection of WGA-HRP into the IO retrogradely filled
agglutinin conjugated to horseradish peroxidase (WGA- many neurons in the classical IO subgroup as well as
HRP; 10 !l, 3%; Sigma, St. Louis, MO) was injected into smaller neurons on the midline, which coincide with the
an eye muscle. In one case (B-61, M. fascicularis) the belly location of IO and SR nontwitch motoneurons, according120 R. WASICKY ET AL. Fig. 1. Twitch and nontwitch motoneuron subgroups in monkey WGA-HRP injection into distal IO muscle, but including some twitch oculomotor nucleus. A: Labelled MR motoneuron subgroups after neurons in the twitch IO subgroup. D: A few twitch neurons, and WGA-HRP injection into the belly of medial rectus muscle. Note that nontwitch motoneurons (in S group), after distal injection of CT into A and B are twitch motoneurons and C group are nontwitch. B: La- SR. A few large twitch motoneurons in the classical IR subgroup were belled IR nontwitch motoneurons in C group after CT injection into filled with CT (arrow). Scale bar # 1 mm. distal IR. C: Nontwitch motoneurons of IO in the S group after to Büttner-Ennever et al. (2001). The midline group of in the S group (Fig. 1D). Since twitch and nontwitch SR nontwitch motoneurons are called here the S group (Fig. motoneurons lie adjacent to each other, when they are 1C). The distal SR injection also filled small motoneurons both retrogradely filled, it can be difficult to differentiate
OCULOMOTOR AFFERENTS TO NONTWITCH MOTONEURONS 121
Fig. 2. Photographs of [3H]leucine injection sites into the abducens nucleus (Z8, Z21) and camera
lucida drawings of afferents labeling at three levels of nIII (caudal to rostral). All cases show a strong
contralateral labeling of twitch and nontwitch motoneuron subgroups. Scale bars # 2 mm.
them, although the twitch motoneurons are on average the adjoining medial longitudinal fasciculus (MLF) to
larger (Büttner-Ennever et al., 2001). In Figure 1D, no cover small islands of motoneurons enclosed between the
large SR motoneurons are labeled in nIII lateral to the S fascicles.
group.
Anterograde labeling from vestibular
Anterograde labeling from abducens nucleus complex
In experiment Z8, radioactively labeled leucine was in-
The vestibular complex can be divided into two main
jected into nVI. The uptake area was almost entirely con-
fined to the nVI boundaries, with slight leakage ventrally cytoarchitectonic areas, a magnocellular and a parvocel-
into a previous electrode track. In case Z21, the tracer was lular region (Epema et al., 1988). The magnocellular divi-
also deposited into nVI. The most rostral part of the nu- sion lies in the center of the vestibular complex; contains
cleus was not filled, but some label might have spread conspicuously large neurons; and includes part of the su-
caudally into rostral nucleus prepositus hyoglossi (pph), perior vestibular nuclei (sv), medial vestibular nuclei
rostral parvocellular medial vestibular nucleus (mvp), and (mv), lateral vestibular nucleus (lv), and spinal vestibular
the supragenual region. The injections sites are shown in nucleus. It is surrounded by the small-celled parvocellular
Figure 2. regions of sv, mv, and lv (for reviews see Büttner-Ennever,
These two experiments gave rise to labeled fibers cross- 1992b; Gerrits, 1990).
ing the midline at the level of nVI and ascending in the In experiment H19, tritiated leucine was deposited in
medial portion of MLF. In each case, fine terminal labeling central magnocellular sv, including the lv, but did not
was found exclusively around the contralateral medial extend medially into the magnocellular medial vestibular
rectus motoneuron subgroups (Figs. 2, 5a). The labeling of nucleus (mvm; Fig. 3). The injection led to anterogradely
the A, B, and C groups was all strong. A continuous band labeled terminals over the classical vertical motoneuron
of terminal labeling was seen in the middle of nIII, be- subgroups, the ipsilateral IR and contralateral IO twitch
tween the IR and the IO subgroups. It passed from the C motoneurons. There was no obvious labeling over the C
group ventrally across nIII to the lateral border of the group or S group, where nontwitch motoneurons lie (Figs.
nucleus and ventrally into the A group. Terminal label 3, 5c). Some midline labeling is visible in H19/174, 178
also extended from the compact part of the A group into (Fig. 3), but it was not of the diffuse character associated122 R. WASICKY ET AL.
Fig. 3. Photographs of [3H]leucine injection sites into mvp (Z30), central sv (H19), and Y group (A4-90)
and camera lucida drawings of afferent labeling at three levels of nIII (caudal to rostral). From mvp and
the Y group, afferents cover both twitch and nontwitch motoneurons subgroups, but, from central sv, the
twitch motoneurons are predominantly targeted. Scale bars # 2 mm.
with terminal labeling and was interpreted as axon lular medial vestibular nucleus (mvp), with no contamina-
branches crossing the midline. Labelled terminals ex- tion of nVI, pph or the mvm (Fig. 3). There was strong
tended into the supraoculomotor area (soa), targeting labeling over the ipsilateral MR A and B subgroups. Dense
parts of the Edinger-Westphal (EW) complex. This label- labeling occurred along the dorsomedial border of the ip-
ing was stronger on the ipsilateral side. silateral nIII including the C group (Figs. 3, 5b). The
A very different pattern of label was observed in case labeling was not confined to the nontwitch motoneuron
Z30, in which the injection was centered on the parvocel- subgroups. It also covered several adjacent cell groups,OCULOMOTOR AFFERENTS TO NONTWITCH MOTONEURONS 123
including parts of the EW complex. The lateral visceral labeling is shown in Figure 5f (case C64) for comparison.
cell column of the EW complex (lvc), the soa, and the The section photographed for Figure 5f is too caudal to
interstitial nucleus of Cajal (iC) were strongly and specif- show the intense labeling of contralateral lvc in this case
ically labeled too. On the ipsilateral side, the MLF con- C64.
tained very few labeled fibers. Those supplying the MR In summary (Fig. 6A), internuclear afferents from the
subgroups ascended laterally to MLF, presumably in scat- nVI region target both the twitch and the nontwitch mo-
tered, poorly visible fibers of the ascending tract of Deiters toneuron subgroups of MR contralaterally, whereas the
(ATD). On the contralateral side there was strong labeling parvocellular mvp projects to them ipsilaterally. In addi-
of fibers in the MLF, which projected mainly into the IR tion, mvp innervates the contralateral vertical twitch sub-
subgroup. On the midline there was significant labeling groups, IR and IO, and the S and C groups, which both
around the region containing IO/SR nontwitch motoneu- contain vertical nontwitch motoneurons. The afferent
rons of the S group (Figs. 3, 5b). pathways from the central magnocellular sv/lv targeted
In case A4-90, the injection was placed in the vestibular only vertical twitch (IO/IR) motoneurons, but the inclu-
complex dorsolateral to the inferior cerebellar peduncle in sion of the Y group in an injection site led to additional
the rostral Y group (Fig. 3). In addition, the spinal vestib- labeling over regions containing nontwitch motoneurons.
ular nucleus and the caudal parvocellular part of sv re- The pretectal area sent axons through nIII, but no termi-
ceived some tracer. There was no involvement of the den- nal projections were found over twitch motoneuron sub-
tate nucleus. The injection gave rise to fibers ascending in groups. Instead, it targeted nontwitch motoneurons in
the contralateral MLF and intense labeling of the classical both the contralateral C group and the S groups over their
SR/IO subgroups in nIII. Fibers continued dorsally along whole extents, as well as other adjacent cell groups, such
the medial margin of nIII and crossed over the midline to as the EW complex and the soa.
the IR motoneurons of the other side (Figs. 3, 5d). On the
midline these axons gave rise to a diffuse pattern of silver
grains, which covered several different regions around the DISCUSSION
midline and dorsomedial borders of the oculomotor nu-
cleus. These regions included the S group, the EW nu- Our results show that twitch and nontwitch motoneu-
cleus, the C groups, and adjacent regions of the soa. ron pools do not receive identical afferent inputs. Affer-
ents from some regions target both motoneuron pools, for
Anterograde labeling from the pretectum example, from the abducens area, Y group, or parvocellu-
In case C9211, the leucine was injected in the centro- lar mvp. Others areas, such as the central magnocellular
caudal pretectum. It included the pretectal olivary nu- sv/lv region, project only to twitch motoneuron subgroups.
cleus (OLN), medial part of the nucleus of the optic tract In contrast, the pretectum projects only to nontwitch mo-
(NOT), nucleus limitans (Li), and portions of the pulvinar toneurons. This result is important; if twitch and non-
(Pu; Fig. 4). In experiment C9004, the injection was more twitch motoneurons have major differences in input, it is
rostral and targeted the anterolateral pretectum. The up- reasonable to predict that they participate in different
take area was large and caudally included portions of the oculomotor functions. This suggests that, in terms of their
NOT, OLN, and rostral superior colliculus (SC). In case roles in eye movements, the nontwitch fibers may have a
A1189, the injection site was more ventral in the central more specialized role than just firing tonically with all
pretectum. It included the NOT, OLN, and posterior and types of eye movements and providing the tonic end of the
anterior pretectal nucleus, and it spread into the interme- final common pathway. Furthermore, these results sup-
diate layers of the SC. port an earlier contention based on motoneuron organiza-
In no case were there any silver grain deposits indica- tion. Specifically, nontwitch motoneurons remain anatom-
tive of a significant axonal termination over the twitch ically separate from the groups of twitch motoneurons,
motoneurons in the classical nIII (Figs. 4, 5e,f). However, and separate neuronal groups tend to receive different
all the pretectal injections gave rise to terminal labeling afferent inputs (Büttner-Ennever et al., 2001).
around nIII. In some cases (A1189) widely distributed, The clustering of fine silver-grain deposits, indicative of
diffuse terminal patterns were observed over the sur- axon terminals over the nontwitch C and S motoneuron
rounding regions (Figs. 4, 5e). The S group, the contralat- groups, is suggestive, but not direct proof, of a premotor
eral C group, and the contralateral lvc of the EW complex input to these neurons. It does not exclude inputs to ad-
were labeled (Figs. 4, 5e). In addition, the trochlear caps jacent structures, whose dendrites may penetrate the C
on the contralateral side, which incorporate nontwitch and S group neuropile, for example, the twitch motoneu-
motoneurons of SO, were also labeled (not shown). Diffuse ron dendrites extending into the soa (Edwards and Hen-
tracer deposits also lay over the soa, mainly contralater- kel, 1978). Furthermore, several patterns of terminal la-
ally. In contrast to the situation for all other pretectal beling extend beyond the boundaries of the C and S groups
cases, in A1189 the whole soa was labeled diffusely, and and definitely contact adjacent structures, in particular,
all the cell groups were labeled bilaterally (Fig. 5e). subdivisions of the EW nuclear complex (Burde, 1988;
In an additional case, reported fully by Büttner- Burde and Williams, 1989; May et al., 1992; Erichsen and
Ennever and colleagues (1996), the leucine injection into May, 2002).
the caudomedial pretectum was centered on the pretectal One drawback of the present and earlier studies is that
olivary nucleus. It resulted in a more specific patch of the technique used to identify nontwitch motoneurons
labeling around the contralateral C group, the S group, labels primarily nontwitch fibers of the inner or global
and the contralateral lvc, but not over the central EW layer of the eye muscle, because the retrograde tracer is
nucleus just dorsal to the C groups. Unlike the case in injected into the distal myotendinous junction, where only
A1189, it did not involve the nPC region or more rostral the global layer of muscle attaches to the sclera (see Fig.
pretectal areas. The relatively isolated C and S group 6B). The outer orbital layer terminates at the level of the124 R. WASICKY ET AL.
Fig. 4. Photographs of [3H]leucine injection sites into the pretectum and camera lucida drawings of
afferent labeling at two levels of nIII (caudal to rostral). All cases show terminal labeling over nontwitch
subgroups (C and S group) and lvc of EW complex, but none over twitch motoneuron subgroups. Scale
bar # 2 mm.
Tenon’s capsule and is thought to insert onto the pulleys predominantly to the motoneurons innervating the global
(Demer et al., 2000; Demer, 2002). Thus, it is uncertain to layer of the eye muscles.
what extent orbital nontwitch endplates are labeled by the
extreme distal injections (Büttner-Ennever et al., 2001). Abducens afferents
The location of the nontwitch motoneurons of the orbital The results confirm that there are inputs to both the
layer remains unclear, and the results shown here apply twitch and the nontwitch MR motoneurons in the oculo-OCULOMOTOR AFFERENTS TO NONTWITCH MOTONEURONS 125
Fig. 6. A: Summary of the different afferents to the twitch mo-
toneurons in nII and to the nontwitch motoneurons in the C and S
groups. B: Schematic drawing of a current hypothesis on the function
of nontwitch motoneurons. Only the nontwitch muscle fibers of the
global layer are associated with palisade endings at the myotendinous
junction. Nontwitch muscle fibers are suited to tonic activity and
could also modulate a proprioceptive feedback signal from the pali-
sade endings.
abducens internuclear neurons, and cell groups of the
paramedian tracts (Büttner-Ennever, 1992a; Büttner-
Ennever and Horn, 1996; Langer et al., 1986). The abdu-
Fig. 5. The differential labeling of twitch and nontwitch motoneu- cens internuclear pathway was shown to contact medial
ron subgroups (C and S groups) in nIII after [3H]leucine injection into rectus motoneuron pools and to form the basis of conjugate
different premotor regions: abducens nucleus (a), mvp (b), sv (c), Y
eye movements, coordinating lateral and medial rectus
group (d), and pretectum (e,f). Case C64 has been described by
Büttner-Ennever et al. (1996) The dotted lines circumscribe the clas- activity (Graybiel, 1977; Carpenter and Batton, 1980;
sical nIII. Scale bar # 1 mm. Büttner-Ennever and Akert, 1981). It is interesting in this
context that the reconstructions of intracellularly stained
reconstructions of identified internuclear neurons in the
abducens nucleus by McCrea et al. (1986) showed crossed
motor nucleus from the abducens nucleus and the imme- projections only to the twitch (A and B) MR subgroups, but
diately surrounding region. The abducens nucleus con- no terminals could be found over the C group. In contrast,
tains several sets of neurons: lateral rectus motoneurons, our injections into the abducens area labeled a significant126 R. WASICKY ET AL.
input to the contralateral C group nontwitch motoneu- tions is a set of neurons lying in central mv, which are
rons. If the C group input did not come from the abducens known to project to the ipsilateral MR subgroups via the
internuclear neurons, it must have come from an addi- ATD (McCrea et al., 1987a). The ATD is thought to carry
tional group of neurons in the abducens area, which head-velocity signals, which generate disconjugate com-
projects specifically, though perhaps not exclusively, to pensatory eye movements (vergence) during utricular ac-
the C group. This seems likely, in that Gamlin and col- tivation from horizontal acceleration (Chen-Huang and
leagues (1989a,b) have described a group of vergence- McCrea, 1998, 1999; Lasker et al., 2002). Single-cell re-
related neurons located near the abducens nucleus that constructions by McCrea et al. (1987a) of four identified
has axons ascending in the MLF. These might be candi- ATD neurons, carrying horizontal signals to the ipsilat-
dates for the C group input labeled by our injections cen- eral nIII MR subgroups, have been shown to terminate
tered on the abducens. strongly in the A and B MR subgroups, but no terminals
were found extending to the C group (McCrea et al.,
Vestibular afferents 1987a). With these findings taken together, it appears
As a result of the studies of Epema et al. (1988), it has that there are cell groups in the parvocellular mvp that
become standard to divide the vestibular complex into a target oculomotor nontwitch motoneurons, but these have
central magnocellular region and an outer parvocellular not yet been labeled intracellularly. Unfortunately, we
region. The former includes the ventrolateral part of mv have no [3H]leucine injections directly into the magnocel-
and central sv, and it is the source of the main vestibular lular mvm, but it is interesting that our preliminary re-
output pathways, for example the secondary canal-related sults with rabies virus as a transsynaptic tracer show that
vestibular axons that project to the oculomotor nucleus. In the magnocellular mvm (as with the magnocellular sv)
contrast, the parvocellular parts of the vestibular complex does not project to the nontwitch motoneurons, albeit of
contain neurons involved in intrinsic vestibular and cere- the abducens nucleus (Ugolini et al., 2001).
bellar connections (Epema et al., 1990; Thunnissen et al.,
1989; for review see Büttner-Ennever, 1992b; Büttner- Afferents from pretectum
Ennever and Gerrits, 2004). These include interconnec- Inputs from the pretectum appear to be a major and, in
tions among medial mv, sv, and pph, as well as their some cases, specific source of afferents to the nontwitch
cerebellar and commissural projections. This network is motoneurons in the C group and the S group. No fine
known to be essential for integrator function, i.e., gaze silver-grain terminal projections over nIII twitch mo-
holding in the oculomotor system (Cannon and Robinson toneurons were observed in nIII: At high magnification,
1987; Straube et al., 1991; Sylvestre et al., 2003). Only the silver labeling shown in Figure 5e,f over nIII can be
vertical canal-related neurons are found in the central seen to be due to axons, not patches of terminals. There
magnocellular sv area. Their connectivity follows the was, in addition, always ample labeling of the densely
“rule” that ipsilateral projections ascending in MLF to packed medium-sized cells of the lvc of the EW complex.
oculomotoneurons are inhibitory, whereas those with The EW complex is composed of several, often indistinct
crossed projections are excitatory (Gacek, 1971; Ito et al., cell groups scattered dorsomedially to nIII (Akert et al.,
1973a,b; Yamamoto et al., 1978; Highstein and Reisine, 1980; Burde and Loewy, 1980; May et al., 1992; Sun and
1979; Precht, 1979). The lv does not project to nIII. Our May, 1993) and, in some reports, a laterally placed lvc of
injections in central sv/lv filled predominantly the magno- the EW complex (Burde, 1988; Burde and Loewy, 1989;
cellular part of sv and labeled terminals over the nIII Büttner-Ennever et al., 1996). In the primate, the lvc of
motoneuron subgroups containing vertical twitch mo- the EW complex was found to contain no preganglionic
toneurons (Yamamoto et al., 1978; Hirai and Uchino, cells (Sun and May, 1993). Most neurons of the dorsome-
1984; Hirai and Hoffmann, 1987; McCrea et al., 1987a). dial EW are larger than the surrounding cells, and the
This finding implies that the nontwitch motoneurons are nucleus contains preganglionic neurons projecting to the
not directly involved in the generation of the vestibuloocu- ciliary ganglion, in part subserving accommodation of the
lar reflexes carried in these pathways. The inclusion of lens (Gamlin et al., 1994). The C group motoneurons lie
mvp or the Y group into the injections labeled diffuse ventral-lateral to EW, immediately adjacent to the nIII
terminals over the nontwitch motoneurons in the midline twitch subgroups. These C group cells were the target of
S and C groups, in addition to projections to the twitch the pretectal afferents, but, at levels rostral to nIII, the C
motoneuron subgroups (Sato and Kawasaki, 1987). This group approaches EW very closely, and common inputs
result speaks for a supplementary tonic role of mvp or the are likely (May et al., 2000; Büttner-Ennever et al., 2001).
Y group in eye muscle control, perhaps in terms of gaze Their close association with each other and the pretectal
holding or visual following (McFarland and Fuchs, 1992; area speaks for a common role, perhaps in aspects of the
Partsalis et al., 1995). near response.
The injection into parvocellular mvp (Fig. 3) labeled The exact source of the pretectal projection to the
ipsilateral inputs to both vertical motoneuron subgroups. nontwitch motoneurons cannot be identified with our
This is to be expected, insofar as McCrea et al. (1987b) leucine injections. However, if the present results are
demonstrated that some secondary vertical canal neurons combined with evidence from WGA-HRP injections into
lie in this region of mv, in a cluster just above the hori- the oculomotor nucleus, and transsynaptic tract tracing
zontal secondary canal neurons. The injections also la- from the medial rectus muscle with tetanus toxin frag-
beled projections to all ipsilateral MR motoneuron sub- ment, the olivary pretectal nucleus (OLN) and the sur-
groups. The premotor inputs from horizontal secondary rounding nucleus of the optic tract (NOT) region appear
vestibular neurons onto MR motoneurons are relayed to be the most likely sources of the input (Büttner-
mainly through abducens internuclear neurons, which Ennever et al., 1996). The OLN contains several sets of
were not included in this injection (McCrea et al., 1980; different-sized neurons (Klooster et al., 1995a,b), and it
Langer et al., 1986). A possible source of our MR projec- is usually associated with pupillary constrictionOCULOMOTOR AFFERENTS TO NONTWITCH MOTONEURONS 127
(Aulhorn, 1967; Gamlin et al., 1995; Pong and Fuchs, cle fibers of the global layer. The importance of such a
2000; Clarke et al., 2003). The neural pathways from putative sensory signal is unclear, but understanding the
the retina to the lvc of the EW complex, via the prete- role of the nontwitch motoneurons might help us to ap-
cum, were traced with a transsynaptic tracer (Kour- preciate its significance.
ouyan and Horton, 1997). The OLN was labeled, and so
were its efferents to the lvc of EW complex, but no
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