THE JOURNAL OF COMPARATIVE NEUROLOGY 250 389-398 (1986)

Neck Muscle Afferent Projections to the

Brainstern of the Monkey: Implications for
the Neural Control of Gaze
DANIEL P. EDNEY AND JOHN D. PORTER
Department of Anatomy, University of Mississippi Medical Center, Jackson, Mississippi
39216

ABSTRACT
Brainstem projections of first-order afferent neurons that innervate the
suboccipital muscles of the monkey have been determined by using the
technique of transganglionic transport of wheat-germ-agglutinin-conjugated
horseradish peroxidase (WGA/HRP)and HRP. Neck muscle afferents distrib-
ute to several distinct regions located within the caudal brainstem and
rostra1 spinal cord. Terminal labeling was heaviest within the ventral por-
tion of the ipsilateral lateral cuneate nucleus. Muscle afferent terminals
also distributed to ventrolateral portions of the pars triangularis division of
the cuneate nucleus. Projections were consistent with the known somato-
topic (i.e., both place and modality) organization of the cuneate nucleus.
Moreover, neck muscle projections to the cuneate nucleus were, in part,
coincident with those previously demonstrated for the extraocular musdes
(Porter: J. Comp. NeuroL 247:133-143, '86). Sparse terminal projections were
noted in the central cervical nucleus. In addition, light terminal labeling
was present in group x of the vestibular complex and in a n ill-defined region
along the lateral margin of the brainstem.
Present observations, which provide the first complete description of the
central distribution of neck muscle afferent neurons in the primate, may
contribute to the known substrate for eyehead coordination.

Key words: eyelhead movement, proprioception, suboccipital muscles

The suboccipital muscle group consists of four small mus-
cles (rectus capitis posterior major and minor, obliquus cap-
itis superior and inferior) that function in fine rotatory
movements of the head. These muscles have an unusually
high content of sensory receptors, inclusive of neuromuscu-
lar spindles and Golgi tendon organs (Richmond and Abra-
hams, '75, '79). Innervation of suboccipital muscle
proprioceptors is provided by neurons located within the C1
dorsal root ganglion. Central projections of suboccipital
muscle afferents in the cat (Bakker et al., '84) involve
central cervical, lateral cuneate, and cuneate nuclei. These
connections provide the anatomical substrate for cervico-
ocular and cervicocollic reflexes that act in concert with
vestibular reflexes to stabilize gaze.
The coordination of eye and head movements is necessary
for acquisition of visual targets and maintenance of stabil-
ity of gaze. Accordingly, coactivation of extraocular and
neck muscles represents the most common behavioral re-
sponse to appearance of a novel visual stimulus (see Bizzi,
'81). The precise role of muscle afferent information in the
neural control of head and eye movements has been the
subject of much debate. Sensory information derived from
neck and eye muscles may participate in gaze (1)by provid-
ing head and eye position signals that are utilized, either
independently or in concert, for visual target localization
and programming of movement and (2) by stabilizing the
fovea upon the newly acquired target by complementing
the vestibulo-ocular and vestibulocollic reflexes. Corollary
discharge and visual sensory feedback represent alterna-
tive sources of such positional cues (Mays and Sparks, '80).
The resolution of similarities and differences in the cen-
tral distribution of extraocular and neck muscle afferents
may provide insight into the role of proprioceptive infor-
mation in the neural control of gaze. The present study
utilized the technique of transganglionic transport of neu-
Accepted March 18, 1986.

0 1986 ALAN R. LISS, INC.

390 D.P. EDNEY AND J.D. PORTER

roanatomical tracers in order to describe the central distri- using a modification of the protocol of Mesulam ('781, as
bution of neck muscle afferents in the monkey. Preliminary described previously (Porter, '86). Sections were mounted
findings have been published elsewhere (Porter and Edney, on slides pretreated with chrom aludgelatin and counter-
'86). stained with 1%neutral red. The distribution of brainstem
terminations of neck muscle afferent neurons was charted
METHODS with reference to nuclear divisions by using a microscope
Brainstem termination sites of neck muscle afferent neu- equipped with a drawing attachment and brightfield, dark-
rons were identified by using the technique of transgan- field, and polarized light illumination. Longitudinal recon-
glionic transport of WGA/HRP and HRP (Mesulam and structions of nuclei containing neck muscle afferent
Brushart, '79). These studies were conducted in four adult recipient zones were made from sections separated by 200-
cynomolgus monkeys (Macaca fasciculuris)3-4 kg in body 400 pm by using a point transfer method. Comparisons
weight. Each animal was sedated with intramuscular ke- between different experimental animals were facilitated by
tamine hydrochloride, and intravenous pentobarbital so- referencing reconstructions to the location of the obex (de-
dium was administered, as needed, in order to maintain an fined herein as the point of confluence of central canal and
appropriate level of surgical anesthesia. Monkeys were then fourth ventricle in the stereotaxic coronal plane of section).
placed in a stereotaxic apparatus. Operations were under-
taken with aseptic conditions and wounds were closed in RESULTS
layers. The dorsal neck region was exposed by a midline Gross anatomical considerations
incision extending from the external occipital protuberance The gross anatomical organization of the dorsal neck
inferiorly to the level of spinous processes of vertebrae C7- region of the monkey is similar to that in man. Muscles of
T1. Following lateral reflection of trapezius and splenius interest for the present study are those that delineate the
capitis muscles, semispinalis capitis was transected a t its suboccipital triangle, specifically obliquus capitis inferior,
midpoint and reflected superiorly to expose the suboccipital obliquus capitis superior, and rectus capitis posterior major.
region. The thick adherent fascia that overlies the suboccip- Obliquus capitis inferior, defining the inferior border of the
ital region was carefully removed to facilitate isolation and triangle, originates from the spine of the axis (C2) and
injection of individual muscles. Selected suboccipital mus- passes laterally and slightly upward to insert on the trans-
cles were injected with 25-50 p1 of a cocktail containing 1% verse process of the atlas (Cl). The lateral margin of the
W G M R P (Sigma) and 10% HRP (Boehringer-Mannheim) suboccipital triangle is formed by the obliquus capitis su-
in distilled water with a 25.~1Hamilton microsyringe. The perior, which arises from the transverse process of the atlas
neuroanatomical tracer was easily visualized within the and passes upward and medially to insert upon the squa-
belly of the injected muscles, thereby allowing us to moni- mous portion of the occipital bone. The triangle is com-
tor and control any leakage subsequent to intramuscular pleted by the rectus capitis posterior major, which arises in
injection. Two monkeys were used for localization of affer- common with the obliquus capitis inferior and courses su-
ent terminals derived from the rectus capitis posterior ma- perolaterally to insert on the occipital bone immediately
jor, superior oblique, and inferior oblique (cases 04-23 and adjacent to the insertion of the obliquus capitis superior.
07-02). Two additional monkeys were used to localize affer- The rectus capitis posterior minor was not studied. To-
ent terminals from the rectus major and one of the oblique gether, the suboccipital muscles serve to rotate the head
muscles (rectus major and the superior oblique in case 06- toward the ipsilateral side and extend the neck at atlanto-
04, rectus major and the inferior oblique in case 06-25). occipital and atlantoaxial joints. Innervation of the suboc-
Warm mineral oil was applied to the region to retard spread cipital muscles is provided by the first cervical spinal nerve,
of the aqueous tracer solution. Prophylactic doses of anti- which emerges through the triangle and emits multiple
biotics were administered and monkeys were placed under small branches to each muscle.
close observation during recovery. Confirmation of injection
site was obtained by anatomical dissection subsequent to Retrograde labeling of neuronal somata
perfusion. Injections of WGA/HRP and HRP into selected suboccipi-
Following survival times of either 48 or 96 hours, mon- tal muscles resulted in retrogradely labeled neurons lo-
keys were deeply anesthetized with pentobarbital sodium, cated within the ventral horn of the C1 spinal cord segment.
heparinized (2,000 IU,i.v.), intubated, and artificially res- Labeled neurons were located predominantly ipsilateral to
pired with 95% oxygen-5% carbon dioxide prior to perfu- the injection site and were distributed across the entire
sion. Monkeys were perfused transcardially by delivering mediolateral extent of the ventral horn. While some labeled
fluid under controlled pressure through a cannula inserted neurons were detected in the ventral horn contralateral to
into the ascending aorta. Physiological saline solution con- the injection site (lamina VIII and IX), it could not be
taining 1%sodium nitrite was introduced, followed by 3 determined with certainty whether these neurons repre-
liters of fixative solution containing 1.25% glutaraldehyde sent motoneurons with decussating axons (Abrahams and
and 1% paraformaldehyde in 0.1 M phosphate buffer (pH Keane, '84) or are the result of spread of tracer from the
7.4). Total perfusion time was 30-60 minutes. Following injection site. In light of recent observations regarding the
perfusions, the brainstem and upper spinal cord were neuronal transport properties of the WGA/HRP tracer (Har-
blocked in situ in the Horsley-Clarke stereotaxic plane, rison et al., '84; Porter et al., '85; Jankowska, '851, some
removed, and immersed in cold (4°C) fixative solution for labeled ventral horn neurons may represent premotor ele-
1.5 hours. Tissue was then transferred to 0.1 M phosphate ments (e.g., Renshaw cells) that contain WGA/HRP by vir-
buffer containing 8% dextrose. The following day 50-pm tue of retrograde transneuronal transport.
coronal sections were obtained with a Vibratome (Lancer) Some retrogradely labeled neurons (six to eight per ani-
and collected in compartmentalized trays. Sections were mal) also were present in the contralateral nucleus of Roller
processed for the histochemical demonstration of HRP by (Fig. l), a component of the perihypoglossal nuclear com-
NECK MUSCLE AFFERENTS
Abbreviations
AP area postrema
cc central cervical nucleus
DPYR pyramidal decussation
I0 inferior olive
N inferior vestibular nucleus
LC lateral cuneate nucleus
MV medial vestibular nucleus
NCpr nucleus cuneatus, pars rotunda
NCpt nucleus cuneatus, pars triangularis
NG nucleus gracilis
NTS nucleus tractus solitarius
PYR pyramid
SPV spinal trigeminal nucleus
10 dorsal motor nucleus of vagus nerve
12 hypoglossal nucleus
plex (Brodal, '83).Labeling density in these neurons was
considerably less than that of punitive motoneurons. Phys-
iological studies (Gresty and Baker, '76) in the cat indicate
that neurons in the perihypoglossal nuclei may represent
premotor elements involved in eyehead movement. Taken
together, these data suggest that neurons in the nucleus of
Roller may represent premotor neurons labeled by retro-
grade transneuronal transport of WGA/HRP tracer. Re-
gions that establish monosynaptic contact with neck muscle
motoneurons (e.g., reticular formation, Peterson et al., '79;
vestibular nuclei, Waespe and Henn, "77) represent candi-
dates €or labeling by a retrograde transneuronal mecha-
nism. Although HRP-labeled somata were absent from other
brainstem areas, interneuronal transfer of lectin-conju-
gated HRP may be a selective process that does not neces-
sarily lead to labeling of all premotor neuron populations
(Porter et al., '85).
Anterograde labeling of synaptic terminals
Injections of selected suboccipital muscles with WGN
HRP and HRP also resulted in transganglionic terminal
labeling that was located ipsilaterally within the lateral
(external, accessory) cuneate nucleus, cuneate nucleus, and
cervical spinal cord (Fig. 2). Light terminal labeling also
was associated with nuclear group x of the ipsilateral ves-
tibular complex. This patterned distribution of afferent ter-
minals was a consistent finding in all experimental cases.
Slight variations in labeling intensity, related to the num-
ber of suboccipital muscles injected, represented the major
interexperimental differences. Since our interest was di-
rected toward a description of recipient zones for the suboc-
cipital muscle group as a whole, mapping of projections
derived from individual muscles was not attempted. The
following descriptions of muscle afferent recipient zones
emphasize features that were present in all experimental
cases. Longitudinal reconstructions of lateral cuneate and
cuneate nuclei were employed in order to depict the rostro-
caudal distribution of neck muscle afferent terminals and
to facilitate their comparison with afferents from other
sources.
Lateral cuneate nucleus. The lateral cuneate nucleus
was the principal termination site for suboccipital muscle
afferents. HRP reaction product characteristic of axon ter-
minals was distributed specifically to ventrolateral portions
of the lateral cuneate nucleus (Figs. 2A-D, 3). Figure 4A
depicts a longitudinal reconstruction of the lateral cuneate
391
\ f
Fig. 1. Charting depicting location of labeled neurons (filled circles at
arrow) within the contralateral nucleus of Roller following injection of
WGA/HRP into the suboccipital muscles. Figure depicts labeled neurons
present in one section of monkey 06-25. This pattern of label is interpreted
as the result of retrograde transneuronal transport of the tracer from neck
muscle motoneurons.
nucleus from a dorsal view. The neck muscle afferent recip-
ient zone occupied much of the rostrocaudal extent of the
lateral cuneate nucleus.
Cuneate nucleus. The cuneate nucleus represented a
second major termination site €or neurons that subserve
neck muscle proprioception. The primate cuneate nucleus
has been divided into two regions, pars triangularis and
pars rotunda, differing in both cytoarchitecture and connec-
tivity (Ferraro and Barrera, '35; Biedenbach, '72; Boivie,
'78; Rustioni et al., '79; Boivie and Boman, '81; Olszewski
and Baxter, '82). HRP reaction product was restricted to
the ventrally located pars triangularis division of the cu-
neate nucleus (Figs. 2, 3). Except for the low levels (i.e., at
or near background) of reaction product observed in case
07-02, the pars rotunda division of this nucleus was devoid
of terminal label. Muscle afferent terminals within pars
triangularis were distributed principally to ventrolateral
regions throughout much of the rostrocaudal extent of the
nucleus. By contrast, medially located patches of reaction
product (Figs. 2B, 4B), seemingly at variance with the es-
tablished somatotopy of this nucleus (Nyberg and Blom-
qvist, '84; Jasmin et al., '851, were observed at some levels.
Figure 4B summarizes data regarding the rostrocaudal ex-
tent of terminal label in the cuneate nucleus.
Injections of suboccipital muscles with WGA/HRP and
HRP also resulted in anterograde labeling overlying an ill-
defined cluster of neurons located ventrolateral to the lat-
eral cuneate and cuneate nuclei (Fig. 5). Such target neu-
rons were located interstitial or immediately dorsal to the
spinal trigeminal tract and appeared distinct from the
neighboring nuclei.
Vestibular complex. In all experimental cases, light ter-
minal labeling was associated with group x of the ipsilat-
era1 vestibular complex. Group x represents a diffuse
collection of rather large neurons that are associated with
the lateral margin of the inferior vestibular nucleus (Bro-
dal, '84). Reaction product indicative of terminals of neck
muscle afferents was observed overlying this nucleus at a
point 200-300 pm rostra1 to the oral pole of the lateral
cuneate nucleus. These observations, while at variance with
392 D.P. EDNEY AND J.D. PORTER

+2.0

MF 04-23

A
p + 0 2

Fig. 2. Charting of the location of WGAMRP and HRP reaction product caudal (El. Stippling (A-E) depicts terminal fields of suboccipital muscle
within the brainstem and spinal cord following injections of the left rectus afferent neurons. Filled circles (D,E) represent labeled neurons in the ven-
capitis posterior major, obliquus capitis superior, and obliquus capitis infe- tral horn of C1. Numbers located at the right-hand edge of each section
rior muscles. Stereotaxic coronal plane sections proceed from rostral (A) to indicate distance, in millimeters, rostral (+)or caudal (-1 to the obex.
NECK MUSCLE AFFERENTS
Fig. 3. Charting at left indicates location of photomicrographs of termi-
nal fields of suboccipital muscle afferents in lateral cuneate and cuneate
nuclei (case 04-23).Brightfield (top) and polarized light (bottom) photomicro-
anatomical studies in the cat (Bakker et al., '84), are consis-
tent with electrophysiological findings (cat; Wilson et al.,
'76).
Spinal cord. Within the spinal cord, the principal locus
of transganglionically transported tracer was the central
cervical nucleus (lamina VII; Fig. 6). This nucleus exhibits
distinctive cytoarchitecture, with round, medium-sized cel-
lular elements, and thus was clearly distinguished from
surrounding structures. Terminal label appeared to be con-
fined to portions of this nucleus residing in the C1 segment;
however, levels caudal to C3 were not examined. In addi-
tion, sparse distribution of HRP reaction product was ob-
served within the substantia gelatinosa of the C1 dorsal
horn in two experimental cases (monkeys 07-02 and 06-04).
DISCUSSION
Injections of WGA/HRP and HRP into primate suboccipi-
tal muscles resulted in terminal labeling within the lateral
cuneate, cuneate, and central cervical nuclei. These data
generally confirm observations made for the suboccipital
muscles of the cat (Bakker et al., '84). Present observations,
however, included two projection sites, group x of the vestib-
393
graphs at right illustrate WGA/HRP reaction product in neck muscle affer-
ent terminals (arrowheads). Photomicrographs: X42.
ular complex and a diffuse region located along the lateral
margin of the brainstem at medullary levels, which were
not observed in the cat (Bakker et al., '84). Since similar
neuroanatomical techniques were used to identify the sub-
occipital muscle afferent recipient zones in the cat and
monkey, the two data sets should be comparable. It is likely
that the additionaI projection sites present in the monkey
represent a species difference related to the potential exis-
tence of different functional roles for neck muscle afferents
in the cat and monkey.
The most impressive transganglionic transport of the
WGA/HRP and HRP tracers was to the ipsilateral lateral
cuneate nucleus. A rnusculotopic (i.e., topographic distribu-
tion of sensory terminals reflecting the positional relation-
ships of skeletal muscles) representation of the upper half
of the body has been demonstrated for the cat lateral cu-
neate nucleus (Nyberg and Blomqvist, '84; Jasmin et al.,
'85). Present findings suggest that a similar musculotopic
organization may exist for the primate lateral cuneate nu-
cleus. The musculotopic organization of neck muscle affer-
ent terminals in the lateral cuneate nucleus, however,
exhibits intersuecies differences. Subocciuital muscles are
~~
394
L S R \I
I triangularis is homologous to the reticular zone of the cat.
I Muscle afferent projections to the cat cuneate nucleus ex-
I
I
I
fobex
I Blomqvist, '84; Jasmin et al., '85). Present observations
I regarding neck muscle afferent projections to the cuneate
I nucleus of the monkey are consistent with the somatotopy
B in the primate (Shriver et al., '68).
c cleus terminate in the somatosensory thalamus, superior
I
-lmm
Fig. 4. Longitudinal reconstructions illustrating the distribution of sub-
occipital muscle afferent terminals in the lateral cuneate nucleus (A) and
cuneate nucleus (Bf of monkev 04-23. Dashed line at right indicates midline,
while solid line at left demarcates lateral margin of Ibrainstem. Letters at
left of each panel refer to levels of corresponding coronal sections in Figure
3. R, rostral; L, lateral.
represented in the ventromedial portion of the nucleus in
the cat (Bakker et al., '84), while occupying its ventrolateral
portion in the monkey (present findings). Although neck
muscle afferent terminals occupied a rather large propor-
tion of the lateral cuneate nucleus, such a finding is not
entirely unexpected since these muscles have a high periph-
eral receptor density (Richmond and Abrahams, '75, '79).
The arrangement of neck muscle afferent projections into a
longitudinally oriented column is consistent with findings
for limb musculature (Nyberg and Blomqvist, '84; Jasmin
et al., '85). Implicit in observations of neck muscle projec-
tions to the lateral cuneate nucleus is the potential for the
subsequent relay of proprioceptive information to the cere-
bellum (cat, Rinvik and Walberg, '75; monkey, Lafleur et
al., '74).
Central projections of neck muscle afferent neurons also
were distributed to the pars triangularis division of the
cuneate nucleus. The cytoarchitectural subdivisions of the
primate cuneate nucleus exhibit clear differences in affer-
ent-efferent organization. Cutaneous regions are repre-
sented in the pars rotunda division and muscles and joints
are represented in the pars triangularis division (Hum-
melsheim et al., '85; Hummelsheim and Wiesendanger,
D.P. EDNEY AND J.D. PORTER
'85). Corresponding findings regarding cytoarchitecture and
connectivity for the cat cuneate nucleus (Kruger et al., '61;
Gordon and Jukes, '64; Kuypers and Tuerk, '64; Dykes et
al., '82) lend support to the notion that the primate pars
hibit a musculotopic pattern of organization in that cau-
dally located muscles are represented ventromedially and
more rostral muscles are represented progressively more
ventrolateral within the reticular zone (Nyberg and
established in the cat in that terminal labeling occupied
the ventrolateral portion of pars triangularis. The muscu-
lotopic pattern is superimposed on a segmental pattern of
cuneate nucleus organization that was previously described
Recent studies have established that the two anatomical
subdivisions of the cat cuneate nucleus have differential
targets in the central nervous system. Projections originat-
ing from the reticular subdivision of the cat cuneate nu-
colliculus, anterior pretectal nucleus, inferior olive, and
pontine nuclei (Hand and Van Winkle, '77; Edwards et al.,
'79; Bull and Berkley, '84; Berkley, '85). Connections in-
volving the pontine nuclei, pretectum, and dorsal accessory
olive (Berkley, '85) provide an anatomical basis for relay of
proprioceptive signals to the cerebellum. While not provid-
ing a complete description of the projection sites of the
primate cuneate nucleus, recent studies (Shriver et al., '68;
Rustioni et al., '79; Cheema et al., '85; HummeIsheim et
al., '85; Hummelsheim and Wiesendanger, '85) demon-
strate similarities with the cat. ~f similar connectivity can
be demonstrated in the monkey it then that
neck muscle projections to the pars triangularis of the CU-
neate nucleus may be relayed, rather directly, to many
areas that have been implicated in the neural control of
gaze (e.g., superior colliculus, flocculus, and vermis of the
cerebellar anterior lobe; see Bizzi, '81; Robinson, '81).Pres-
ent observations that neck muscle terminals within the
cuneate nucleus are partially coextensive with those of the
extraocular muscles (present findings; Porter, '86) lend sup-
port to the notion that integration of afferent information
from these two sources may contribute to the neural control
of gaze.
Projections involving the central cervical nucleus provide
a n additional means by which neck muscle afferent infor-
mation may be relayed to the cerebellum. The central cer-
vical nucleus receives direct input from upper cervical
dorsal roots (Shriver et al., '68; Hirai et al., '84) and, in the
cat, sends bilateral projections to the vermis of cerebellar
lobules I-VII (principally lobules I and 11; Wiksten and
Grant, '83).Present findings demonstrate that spinal affer-
ents to the central cervical nucleus arise, at least in part,
from the dorsal neck muscles. It appears, however, that this
nucleus may pIay less of a role in distribution of primate
suboccipital muscle afferent information than has been
demonstrated for the cat (Bakker et al., '84), since only
light terminal fields were observed a t this site in the mon-
key. The central cervical nucleus also serves as a pathway
for transmission of vestibular information to the cerebel-
lum (Hirai et al., '78), thereby providing a mechanism for
interaction of vestibular and proprioceptive signals. Neck
NECK MUSCLE AFFERENTS 395

Fig. 5. Charting a t left indicates location of WGA/HRP labeled terminals presence of label overlying cluster of small diameter neurons located near
in region adjacent to lateral cuneate and cuneate nuclei (case 04-23).Bright- lateral margin of brainstem (arrowheads). Photomicrographs: x42.
field (top) and polarized light (bottom) photomicrographs at right illustrate

Fig. 6. Brightfield (A) and polarized light (B) photomicrographs illustrat- tomicrographs taken at rostrocaudal level approximately the same as Fig-
ing WGA/HRP reaction product in the central cervical nucleus at C 1 spinal ure 3E. Arrows indicate location of central canal. X 4 2 .
cord level subsequent to injection of suhoccipital muscles (case 06-25).Pho-
396
NECK EXTRAOCULAR
MUSCLE MUSCLE
Fig. 7. Summary diagram comparing terminal distribution of muscle
afferents (stippling) from neck and extraocular muscles in the primate
cuneate nucleus. Longitudinal reconstructions represent composites of all
experimental cases. Terminal labeling occupied the extreme ventrolateral
corner of pars triangularisfor both neck and extraccular muscles. Extraocu-
lar muscle data from Porter ('86).
muscle afferent projections to group x of the vestibular
complex may serve a similar function (Wilson et al., '76).
Functional considerations
While neck muscle motoneurons receive monosynaptic
input from homonymous sensory receptors, the synaptic
efficacy of such signals is rather low (Abrahams, '77; Abra-
hams et al., '79; Rapoport, '79; Keirstead and Rose, '84).
Thus it is unlikely that neck muscle afYerents exert the
degree of direct influence upon motoneurons that has been
noted for muscle afferents at lumbosacral spinal cord levels.
Instead, the principal function of neck muscle propriocep-
tors appears to be exerted through other neurons in the
spinal cord and brainstem. Thus, it would appear that infor-
mation derived from neck muscle proprioceptors, rather
than serving a primary role in reflex modulation of moto-
neuron firing rate, is important for a more global coordina-
tion of muscle activity. Absence of significant monosynaptic
feedback to neck muscle motoneurons, a characteristic
shared with the oculomotor system (Baker and Precht, '72),
may be related to the minimal requirements for external
load compensation in this system.
Present findings, taken together with information regard-
ing the projections of extraocular muscle afferents (Porter,
'86),indicate that neck and extraocular muscle recipient
zones partially overlap in rostra1 portions of the cuneate
nucleus (Fig. 7). This finding is not altogether surprising
since coordination of eye and head movement systems must
be achieved in some manner. It remains to be determined
whether extraocular and neck muscle afferent projections
indeed converge on the same neurons or merely share over-
lapping spatial domains with no interaction between the
two signals at this level.
The notion of the ultimate convergence of eye and neck
muscle afferent signals is supported by the identification of
such interactions in the frontal eye fields and superior
colliculus of the cat (Abrahams and Rose, '75; Dubrovsky
and Barbas, '77; Barbas and Dubrovsky, '81a,b). Further-
more, interaction of neck and extraocular muscle afferent
information with visual andor vestibular sensory signals
occurs within the cerebellar vermis (lobule V; Berthoz and
D.P. EDNEY AND J.D. PORTER
Llinas, '74) and flocculus Wilson et al., '76; Kimura and
Maekawa, '81; Noda, '81).Clearly, these areas are critical
not only for the neural control of normal gaze mechanisms,
but also in adaptive regulation of such mechanisms (see
Robinson, '81).In order to acquire a visual target, and
maintain stability of fixation upon the target, the coordi-
nated action of eye and head movement systems is re-
quired. Proprioceptive information derived from neck and
extraocular muscles can participate in motor control by
acting a t two levels. First, stabilization of a visual target
upon the fovea is accomplished by vestibulo-ocular and
vestibulocollic reflexes. Neck muscle afferent involvement
in the modulation of these reflexes is well documented and
takes the form of cervico-ocular and cervicocollic reflexes
(Hikosaka and Maeda, '73; Gresty, '76; Barmack et al., '81;
Bilotto et al., '82; Bohmer and Henn, '83; Ezure et al., '83;
Peterson et al., '85). For example, the cervicocollic reflex
complements vestibular-driven reflexes by producing com-
pensatory movements in response to head rotations that
fall below the threshold of the vestibulocollic reflex (Peter-
son et al., '85). The role of extraocular muscle afferents in
stabilization of gaze is less well established (Fiorentini and
Maffei, '77). Second, proprioception may contribute to the
head and eye position signals required in movement initia-
tion. While previous studies have demonstrated that eye
position signals provided by corollary discharge are suffi-
cient for spatial localization of visual targets (Guthrie et
al., '831,proprioception may provide positional information
to eyehead movement initiation centers for as-yet-undeter-
mined functions. The presence of muscle afferent informa-
tion on tectospinal and tectoreticular neurons (Abrahams
and Rose, '79, neurons that are presumed to convey the
output of the deep layers of the superior colliculus to the
brainstem circuitry responsible for generation of neck and
eye movements, lends support to such a claim. Finally,
afferent information derived from extraocular and neck
muscles may provide velocity or positional cues in situa-
tions for which, due to peripheral pathology andor pertur-
bation of the motor plant (i.e., the motoneurons and muscles
they innervate), corollary discharge does not accurately
reflect actual change in eyehead position.
ACKNOWLEDGMENTS
The technical assistance of Virginia Taylor and Esther
McMahon is greatly appreciated. We are also grateful to
Drs. Karen Berkley, Duane Haines, and Norman Capra for
their comments on a n earlier version of the manuscript.
These studies were supported by US. Public Health Service
grant 1 ROf EY06464 from the National Eye Institute to
J.D.P. D.P.E. was supported by a Medical Student Research
Fellowship from the University Medical Center.
LITERATURE CITED
Abrahams, V.C. (1977) The physiology of neck muscles; Their role in head
movement and maintenance of posture. Can. J. Physiol. Pharmacol.
55:332-338.
Abrahams, V.C., and P.K. Rose (1976) Projections of extraocular, neck mus-
cle and retinal afferents to superior colliculus in the cat: Their connec-
tions to cells of origin of tectospinal tract. J. Neurophysiol. 38:lO-18.
Abrahams, V.C., and J. Keane (1984) Contralateral, midline and commis-
sural motonebrons of neck muscles: A retrograde HRP study in the cat.
J. Comp. Neurol. 223:448-456.
Abrahams, V.C., G. Anstee, F.J.R. Richmond, and P.K. Rose (1979) Neck
muscle and trigeminal input to the upper cervical cord and lower me-
dulla of the cat. Can. J. Physiol. Pharmacol. 57:642-661.
Baker, R., and W. Precht (1972)Electrophysiological properties of trochlear
NECK MUSCLE AFFERENTS
motoneurons as revealed by IVth nerve stimulation. Exp. Brain Res.
14.127-157,
Bakker, D.A., F.J.R. Richmond, and V.C. Abrahams (1984) Central projec-
tions from cat suboccipital muscles: A study using transganglionic
transport of horseradish peroxidase. J. Comp. Neurol. 228.409-421,
Barbas, H.. and B. Dubrovsky (1981a) Excitatory and inhibitory interac-
tions of extraocular and dorsal neck muscle afferents in the cat frontal
cortex. Exp. Neurol. 74.51-66.
Barbas, H., and B. Dubrovsky (1981b)Central and peripheral effects of tonic
vibratory stimuli to dorsal neck and extraocular muscles in the cat.
Exp. Neurol. 74.67-85,
Barmack, N.H., M.A. Nastes, and V.E. Pettorossi (1981) The horizontal and
vertical cervico-ocular reflexes of the rabbit. Brain Res. 224.261-278.
Berkley, K.J. (1985) Multiple systems diverging from the dorsal column
nuclei in the cat. In M. Rowe and W.D. Willis (eds): Development,
Organization, and Processing in Somatosensory Pathways. New York:
Alan R. Liss, Inc., pp. 191-202.
Berthoz, A., and R. Llinas (1974)Afferent neck projection to the cat cerebel-
lar cortex. Exp. Brain Res. 2Or385-401.
Biedenbach, M.A. (1972)Cell density and regional distribution of cell types
in the cuneate nucleus of the rhesus monkey. Brain Res. 45.1-14.
Bilotto, G., R.H. Schor, Y. Uchino, and V.J. Wilson (1982) Localization of
proprioceptive reflexes in the splenius muscle of the cat. Brain Res.
238.217-221.
Bizzi, E. (1981) Eye-head coordination. In V. Brooks (ed)Handbook of Phys-
iology, Sect. 1, Vol. 11: Motor Control, Part 2. Bethesda: American Phys-
iological Society, pp. 1321-1336.
Bohmer, A., and V. Henn (1983) Horizontal and vertical vestibulo-ocular
and cervico-ocular reflexes in the monkey during high frequency rota-
tion. Brain Res. 277t241-248.
Boivie, J. (1978)Anatomical observations on the dorsal column nuclei, their
thalamic projection and the cytoarchitecture of some somatosensory
thalamic nuclei in the monkey. J. Comp. Neurol. 178:17-48.
Boivie, J., and K. Boman (1981)Termination of a separate (proprioceptive?)
cuneothalamic tract from external cuneate nucleus in monkey. Brain
Res. 224r235-246.
Brodal, A. (1983) The perihypoglossal nuclei in the macaque monkey and
chimpanzee. J. Comp. Neurol. 218:257-269.
Brodal, A. (1984) The vestibular nuclei in the macaque monkey. J. Comp.
Neurol. 227.252-266.
Bull, M.S., and K.J. Berkley (1984) Differences in the neurons that project
from the dorsal column nuclei to the diencephalon, pretectum and tec-
tum in the cat. Somatosens. Res. 1.281-300.
Cheema, S., A. Rustioni, and B.L. Whitsel (1985) Sensorimotor cortical
projections to the primate cuneate nucleus. J. Comp. Neurol. 240:
196-211.
Dubrovsky, B.O., and H. Barbas (1977) Frontal projections of dorsal neck
and extraocular muscles. Exp. Neurol. 55680493.
Dykes, R.W., D.D. Rasmusson, D. Sretavan, and N.B. Rehman (1982) Sub-
modality segregation and receptive-field sequences in cuneate, gracile
and external cuneate nuclei of the cat. J. Neurophysiol. 47.389416.
Edwards, S.B., C.L. Ginsburgh, C.K. Henkel, and B.E. Stein (1979)Sources
of subcortical projections to the superior colliculus in the cat. J. Comp.
Neurol. 184.309-330.
Ezure, K., K. Fukushima, R.H. Schor, and V.J. Wilson (1983)Compartmen-
talization of the cervicocollic reflex in cat splenius muscle. Exp. Brain
Res. 51.397404.
Ferraro, A., and S.E. Barrera (1935)The nuclei of the posterior funiculi in
macacus rhesus: An anatomic and experimental investigation. Arch.
Neurol. Psychiat. 33r262-275.
Fiorentini, A., and L. Maffei (1977) Instability of the eye in the dark and
proprioception. Nature 269r330-331.
Gordon, G., and M.G.M. Jukes (1964)Dual organization of the exteroceptive
components of the cats gracile nucleus. J. Physiol. (Lond.) I73r263-290.
Gresty, M.A. (1976) A reexamination of the “neck reflex” eye movements
in the rabbit. Acta Otolaryngol. 81r386-394.
Gresty, M., and R. Baker (1976) Neurons with visual receptive field, eye
movement and neck displacement sensitivity within and around the
nucleus prepositus hypoglossi in the alert cat. Exp. Brain Res. 24:
429433.
Guthrie, B.L., J.D. Porter, and D.L. Sparks (1983) Corollary discharge pro-
vides accurate eye position information to the oculomotor system. Sci-
ence 221.1193-1195.
397
Hand, P.J., and T. Van Winkle (1977)The efferent connections of the feline
nucleus cuneatus. J. Comp. Neurol. 171.83-110.
Harrison, P.J., H. Hultborn, E. Jankowska, R. Katz, B. Storai, and D.
Zytnicki (1984) Labelling of interneurons by retrograde transsynaptic
transport of horseradish peroxidase from motoneurons in rats and cats.
Neurosci. Lett. 4515-19.
Hikosaka, O., and M. Maeda (1973) Cervical effects on abducens motoneu-
rons and their interaction with vestibulo-ocular reflex. Exp. Brain Res.
18512-530.
Hirai, N., T. Hongo, and S. Sasaki (19781 Cerebellar projection and input
organizations of the spinocerebellar tract arising from the central cer-
vical nucleus in the cat. Brain Res. 157.341-345.
Hirai, N., T. Hongo, S. Sasaki, M. Yamashita, and K. Yoshida (1984) Neck
muscle afferent input to spinocerebellar tract cells of the central cervical
nucleus in the cat. Exp. Brain Res. 55:286-300.
Hummelsheim, H., and M. Wiesendanger (1985) Neuronal responses of
medullary relay cells to controlled stretches of forearm muscles in the
monkey. Neuroscience 16.989-996.
Hummelsheim, H., R. Wiesendanger, M. Wiesendanger, and M. Bianchetti
(1985) The projection of low-threshold muscle afferents of the forelimb
to the main and external cuneate nuclei of the monkey. Neuroscience
16.979-987.
Jankowska, E. (1985) Further indications for enhancement of retrograde
transneuronal transport of WGA-HRP by synaptic activity. Brain Res.
341.403-408.
Jasmin, L., J. Courville, and D.A. Bakker (1985) Afferent projections from
forelimb muscles to the external and main cuneate nuclei in the c a t A
study with transganglionic transport of horseradish peroxidase. Anat.
Embryol. 171r275-284.
Keirstead, S.A., and P.K. Rose (1984) An examination of muscle spindle
afferent motoneuron connectivity in the upper cervical spinal cord. Can.
J. Physiol. Pharmacol. 62rAxvii.
Kimura, M., and K. Maekawa (1981) Activity of flocculus Purkinje cells
during passive eye movements. J. Neurophysiol. 46:1004-1017.
Kruger, L., R. Siminoff, and P. Witkovsky (1961) Single neuron analysis of
dorsal column nuclei and spinal nucleus of trigeminal in cat. J. Neuro-
physiol. 24:333-349.
Kuypers, H.G.J.M., and J.C. Tuerk (1964) The distribution of the cortical
fibres within the nuclei cuneatus and gracilis in cat. J. Anat. 98:
143-162.
Lafleur, J., J. De Lean, and L.J. Poirier (1974) Physiopathology of the
cerebellum in the monkey. Part 1. Origin of cerebellar afferent nervous
fibers from the spinal cord and brainstem. J. Neurol. Sci. 22.471-490.
Mays, L.E., and D.L. Sparks (1980)Saccades are spatially, not retinocentri-
cally, coded. Science 208:1163-1165.
Mesulam, M.-M. (1978) Tetramethylbenzidine for horseradish peroxidase
neurohistochemistry: A noncarcinogenic blue reaction product with
superior sensitivity for visualizing neural afferents and efferents. J.
Histochem. Cytochem. 26.106-117.
Mesulam, M.-M., and T.M. Brushart (1979) Transganglionic and antero-
grade transport of horseradish peroxidase across dorsal root ganglia: A
tetramethylbenzidine m e t h d for tracing central sensory connections of
muscles and peripheral nerves. Neuroscience 4:1107-1117.
Noda, H. (1981) Visual mossy fiber inputs to the flocculus of the monkey.
AM. N.Y. Acad. Sci. 374:465475.
Nyberg, G., and A. Blomqvist (1984)The central projection of muscle affer-
ent fibres to the lower medulla and upper spinal cord An anatomical
study in the cat with the transganglionic transport method. J. Comp.
Neurol. 230:99-109.
Olszewski, J., and D. Baxter (1982) Cybarchitedure of the Human Brain
Stem. New York S. Karger.
Peterson, B.W., N.G. Pitts, and K. Fukushima (1979)Reticulospinal connec-
tions with limb and axial motoneurons. Exp. Brain Res. 36~1-20.
Peterson, B.W., J. Goldberg, G. Bilotto, and J.H. Fuller (1985)Cervicocollic
reflex: Its dynamic properties and interaction with vestibular reflexes.
J. Neurophysiol. 84.90-109.
Porter, J.D. (1986) Brainstem terminations of extraocular muscle primary
afferent neurons in the monkey. J. Comp. Neurol. 247.133-143,
Porter, J.D., and D.P. Edney (1986) Comparison of the central projections of
extraocular and dorsal neck muscle afferents in the monkey: Implica-
tions for the neural control of gaze. Invest. Ophthalmol. Vis. Sci. (Suppl.)
27.60.
Porter, J.D., B.L. Guthrie, and D.L. Sparks (1985) Selective retrograde
398
transneuronal transport of wheat germ aggl utinin-conjugated horserad-
ish peroxidase in the oculomotor system. Exp. Brain Res. 57:411-416.
Rapoport, S. (1979) Reflex connexions of motoneurones of muscles involved
in head movement in the cat. J. Physiol. (Lond.) 289:311-327.
Richmond, F.J.R., and V.C. Abrahams (1975) Morphology and distribution
of muscle spindles in dorsal muscles of the cat neck. J. Neurophysiol.
38:1322-1339.
Richmond, F.J.R., and V.C. Abrahams (1979) What are the proprioceptors of
the neck? In R. Grant and 0. Pompeiano (eds): Progress in Brain Re-
search, Vol. 50, Reflex Control of Posture and Movement. Amsterdam:
Elsevier, pp. 245-254.
Rinvik, E., and F. Wahlberg (1975) Studies on the cerebelIar projections
from the main and external cuneate nuclei in the cat by means of
retrograde axonal transport of horseradish peroxidase. Brain Res.
95r371-381.
Robinson, D.A. (1981) Control of eye movements. In V. Brooks (ed): Hand-
book of Physiology, Sect. 1, Vol. I 1 Motor Control, Part 2. Bethesda:
D.P. EDNEY AND J.D. PORTER
American Physiological Society, pp 1275-1320.
Rustioni, A., N.L. Hayes, and S. O’Neill (1979) Dorsal column nuclei and
ascending spinal afferents in macaques. Brain 102:95-125.
Shriver, J.E., B.M. Stein, and M.B. Carpenter (1968)Central projections of
spinal dorsal roots in monkey. I. Cervical and upper thoracic dorsal
roots. Am. J. Anat. 123:27-74.
Waespe, W., and V. Henn (1977) Neuronal activity in the vestibular nuclei
of the alert monkey during vestibular and optokinetic stimulation. Exp.
Brain Res. 27:523-538.
Wiksten, B., and G. Grant (1983) The central cervical nucleus in the cat. IV.
Afferent fiber connections: An experimental anatomical study. Exp.
Brain Res. 51:405-412.
Wilson, V.J., M. Maeda, J.I. Franck, and H. Shimazu (1976) Mossy fiber
neck and second-order labyrinthine projections to cat flocculus. J. Neu-
rophysiol. 39:301-310.