THE ANATOMICAL RECORD 222:95-102 (1988)

Nerve Pathways Between the Pterygopalatine

Ganglion and Eye in Cats
TON LIN, PATRICIA A. GRIMES, AND RICHARD A. STONE
Department of Ophthalmology, University of Pennsylvania School of Medicine and Scheie
Eye Institute, Philadelphia, PA 19104

ABSTRACT By dissection of thiocholine-stained orbital preparations, it has been

determined that three different nerve pathways link the pterygopalatine ganglion
and the eye in cats. 1)Nerves from the proximal half of the ganglion join a plexus of
nerves and ganglion cells in the rete mirabile of the maxillary artery. Branches of
the internal carotid nerve also supply this plexus. Fine nerves from the plexus travel
to the optic nerve and then to the eye, accompanying both the nasociliary nerve that
passes through the rete and the ciliary arteries that arise from the rete. 2) One or
more nerves from the nerve of the pterygoid canal and from a prominent accessory
ganglion near the orbital apex course to the inferior optic nerve surface at the optic
foramen; these then run distally along the optic nerve to fuse with ciliary nerves or
to accompany ciliary arteries entering the eye. 3) Other nerves from the pterygopa-
latine ganglion travel medially around the extraocular muscle cone to join the eth-
moidal and infratrochlear branches of the nasociliary nerve; some nerves from the
ganglion then take a retrograde course to the optic nerve, where they join ciliary
nerves or arteries to the eye. All three pathways may transmit sympathetic, para-
sympathetic and somatic sensory nerve fibers.

Parasympathetic nerve fibers in the eye arise from
two ganglia, the ciliary and pterygopalatine, and from
scattered accessory cells. The pterygopalatine ganglion
is the most recently recognized of these sources. In rab-
bits, monkeys, and man, rami orbitales from the pter-
ygopalatine ganglion join branches of the internal carotid
nerve to form a retro-orbital plexus surrounding the
oculomotor, trochlear, ophthalmic, and abducens nerves
just before they enter the orbit (Ruskell, 1965, 1970a).
In rabbits and monkeys (Ruskell, 1965, 1970b), fine
nerves from this plexus supply the eye. A similar path-
way between the pterygopalatine ganglion and the eye
has been identified recently in rats (Kuwayama et al.,
1987).
The pterygopalatine ganglion contains many vaso-
active intestinal polypeptide-like (VIP-like) immuno-
reactive neurons (Uddman et al., 1980a; Hara et al.,
1985) and may be a source of VIP nerves found in var-
ious cephalic structures, including the eye. In the cat,
VIP nerves in the posterior uvea of the eye disappear
following extirpation of the pterygopalatine ganglion
(Uddmann et al., 1980b), but neural pathways between
the ganglion and the eye have not been identified an-
atomically in this species. To provide a basis for further
analysis of the pterygopalatine contribution to the ocu-
lar innervation, we describe the results of dissections
of the cat orbit that identify three routes by which nerves
of the pterygopalatine ganglion reach the eye.
METHODS
We obtained orbital tissues from 19 cats euthanized
under deep chloralose anesthesia as part of unrelated
ventricle with 0.85%NaCl solution prior to death. After
lateral orbitotomy and craniotomy, the complete orbital
contents, including the pterygopalatine ganglion and
maxillary nerve, were removed together with the in-
tracranial portions of the second through sixth cranial
nerves. The preparations were fixed by immersion in
4% formaldehyde for 30 min and washed overnight in
water.
After careful removal of extraneous tissue, we stained
the preparations by a thiocholine method for detection
of cholinesterase activity (Koelle and Friedenwald, 1949)
adapted for whole mounts of nerves and ganglia (Gienc,
1977; Kuwayama et al., 1987). The stained tissues were
dissected to identify and trace nerves from the ptery-
gopalatine ganglion to the eye.
Specimens of the rete mirabile and of some nerves
passing from the pterygopalatine ganglion to the eye
were dissected from three additional cats for histolog-
ical examination. The animals, under deep chloralose
anesthesia, were perfused with Zamboni’ssolution (Ste-
fanini et al., 1967). The tissues were postfixed in 2%
osmium tetroxide, dehydrated in graded alcohols, and
embedded in Araldite. Tissue sections, 1or 2 pm thick,
were stained with methylene blue-azure B and ex-
amined with light microscopy.
RESULTS
The histochemical method for cholinesterase activity
as applied here to partially dissected orbital prepara-
tions effectively stains autonomic postganglionic nerves
arising from both the pterygopalatine ganglion and the
~

experiments. The cats were perfused through the left Received November 2, 1987; accepted February 4, 1988.

0 1988 ALAN R. LISS, INC.

96 T. LIN ET AL.
Internal
ethmoidal
artery
maxillary ‘Rete
artery m Ira bile
Fig. 1. Drawing of the pterygopalatine ganglion and its nerve pathways
to the eye. The rete mirabile is cut away and offset from contiguous
structures to allow visualizaiton of all connections. Thiocholine-stained
autonomic nerves are represented by thick black lines, and the plexus
of fine stained fibers within arterial walls is indicated by cross-hatching.
The numbers indicate each of the three pathways from the ganglion to
superior cervical sympathetic ganglion. Postganglionic
nerves from the ciliary ganglion are not stained, how-
ever, presumably because in cats the axons of ciliary
ganglion cells are myelinated (Christensen, 1935-1936).
Somatic sensory and motor nerves are not stained by
this procedure. The histochemical reaction greatly fa-
cilitates identification of fine autonomic nerves and mi-
croganglia.
The pterygopalatine ganglion of the cat rests on the
pterygoid muscle that forms the posterior orbital floor,
approximately one-third of the way between the apex
and inferior margin of the orbit. The ganglion is posi-
tioned between the medial orbital wall and the orbital
portion of the maxillary nerve and lies just posterola-
teral to the sphenopalatine foramen. The nerve of the
pterygoid canal conveys preganglionic parasympathetic
nerves that synapse in the ganglion; it also carries post-
ganglionic sympathetic nerve fibers and possibly sen-
sory fibers of facial nerve origin, both of which pass
through the ganglion without synapse. Additional sen-
sory and sympathetic fibers from sphenopalatine
branches of the maxillary nerve also traverse the gan-
glion (Christensen, 1934).
Figure 1 diagramatically illustrates and Figure 2
demonstrates the relation of the ganglion and its
branches to the maxillary nerve and artery. Large and
small nerves from the distal end of the ganglion supply
the nose, palate, and anterior orbital structures. Other
nerves branching from the proximal end of the ganglion
or from the nerve of the pterygoid canal, central to the
ganglion, take a retrograde course towards the orbital
the eye: 1. Nerves to the rete mirabile. 2. Nerves to the inferior optic
nerve sheath. 3. Nerves connecting with terminal branches of the na-
sociliary nerve. The thin dashed lines show the limits of the extraocular
muscle cone, omitted for simplicity. V-1, ophthalmic nerve; V-2, m d -
lary nerve; Vidian nerve, nerve of the pterygoid canal.
apex. These nerves divide and anastamose as they travel
caudally and occasionally include small ganglion cell
aggregates at the junction points. We identified three
pathways by which some of these posteriorly directed
nerves reach the eye (Figs. 1, 2).
1 . Nerves to the rete mirabile. As they enter the orbit,
the maxillary artery and nerve are surrounded by a
large rete mirabile formed from two or three branches
of the maxillary artery. Arterial branches leaving the
rete communicate with the cranial circulation and also
supply the eye (Davis and Story, 1943; Gillilan and
Markesbery, 1963). The intraorbital portion of the rete
extends from the foramen rotundum to the optic fora-
men and overlies the nerve of the pterygoid canal as it
enters the orbit. Branches from the nerve of the pter-
ygoid canal and nerves from the proximal end of the
pterygopalatine ganglion enter the rete and join a com-
plex nerve plexus within it (Fig. 3A). The stained nerves
of the plexus divide and anastamose frequently between
the rete vessels. Small aggregates of ganglion cells com-
monly are seen in nerves entering the plexus as well
as within the plexus (Fig. 4). In addition, the rete ves-
sels themselves, the maxillary artery, and all arterial
branches arising from the rete are invested with a dense
intramural plexus of fine stained nerve fibers.
Sympathetic nerves also join the nerve network in
the arterial rete. Two or more branches of the internal
carotid nerve beneath the trigeminal ganglion (Fig. 3B)
course forward between the ophthalmic and maxillary
nerves and enter the external rete mirabile at its caudal
edge. Ramifications of the sympathetic nerves mix with
 NERVES FROM PTERYGOPALATINE GANGLION TO EYE
Fig. 2. Relation of the pterygopalatine ganglion (PPG)to the m d a r y
nerve (V-8) and artery on the orbital floor. The proximal portions of the
maxillary nerve and artery and the rete mirabile have been dissected
the nerve plexus of the rete. In some preparations, sym-
pathetic nerve branches are seen to join small ganglia
located in the caudal portion of the rete.
Because of the complexity of the nerve plexus, it is
impossible to trace the course of individual nerves in-
side the rete. Therefore, we could not establish with
certainty whether sympathetic nerves link with nerves
from the pterygopalatine ganglion, which nerves join
with the microganglia of the plexus, or to what extent
plexus nerves innervate the arterial walls. However,
we observed that fine nerves from the plexus travel to
the superior surface of the optic nerve in association
with the nasociliary nerve passing through the rete and
with the ciliary artery arising from the rete (Fig. 3C).
These nerves from the plexus then course anteriorly
along the optic nerve to enter the eye.
2. Nerves to the inferior optic nerve sheath. Near the
orbital apex there is usually a small mass of ganglion
cells associated with the nerve of the pterygoid canal.
A branch from this accessory ganglion, together with
other nerves running caudally from the pterygopalatine
ganglion, takes a dorsal course to the inferior surface
of the optic nerve near the optic foramen (Fig. 5). One
or more of the nerves accompany the internal ethmoidal
artery from the orbit through the optic foramen to the
cranial cavity. The remaining nerve or nerves turn to
course along the inferior surface of the optic nerve and
ultimately enter the eye.
3. Nerves connecting with terminal branches of the
nasociliary nerve. As many as 5-10 nerve branches from
the pterygopalatine ganglion travel medially under and
around the extraocular muscle cone. They join the eth-
moidal and infratrochlear branches of the nasociliary
nerve that emerge from beneath the medial border of
97
away. The numbers indicate the approximate sites of origin of the three
nerve pathways to the eye and correspond to those of the drawing in
Figure 1. NPC,nerve of the pterygoid canal. Magnification bar, 5 mm.
the superior rectus muscle (Fig. 6). Most of the nerves
from the pterygopalatine ganglion fuse with or accom-
pany the ethmoidal nerve or, to a lesser extent, the
infratrochlear nerve in their peripheral distributions.
Some, however, travel centrally along the nasociliary
nerve branches to the superior surface of the optic nerve,
where they join with ciliary nerves or arteries supplying
the eye.
Nerves from the pterygopalatine ganglion reaching
the optic nerve by all three of these pathways ultimately
form an interdigitating network of fine nerves that sur-
round and accompany the ciliary artery; these nerves
remain clearly distinct from the intramural innervation
of the vessel (Fig. 7). Some of the nerves join ciliary
nerves close to the eye, but most enter the globe along
the inferior surface of optic nerve with branches of the
ciliary artery.
The only nerves traveling between the pterygopala-
tine ganglion and the eye identifiable with certainty in
unstained orbital dissections are the nerves on the in-
ferior optic nerve surface. On the basis of histological
sections of the optic nerve within the orbital apex region
from five orbits of three cats, the number of nerves on
the inferior optic nerve surface have been determined
to range from two to five. The majority of axons in these
nerves are unmyelinated, but 15 of 17 examined nerves
contained a modest number of myelinated fibers meas-
uring between 1 p.m and 6 p.m in diameter (Fig. 8).
DISCUSSION
The fine nerves from the pterygopalatine ganglion
that supply the cat eye have not been noted in previous
anatomical descriptions of ocular parasympathetic
nerves in this animal (Cristensen, 1935-1936; Lele and
98 T. LIN ET AL.

Fig. 3. Pathway 1: Nerves to the rete mirabile. A: Nerves from the blood vessels and other nerves in this region. One or more of the sym-
proximal end o f the pterygopalatine ganglion and from the nerve o f the pathetic nerves (arrowhead) pass rostrally to enter the rete mirabile and
pterygoid canal enter the rete mirabile, where they join a complex plexus join the nerve plexus within it. C: Nerves (arrowheads) from the plexus
of nerves containing microganglia (arrowheads) and isolated ganglion accompany the nasociliary nerve (NCN) and ciliary artery (arrow) as
cells. The nerve of the pterygoid canal (arrow) is cut close to the point they leave the rete and travel with them to the optic nerve (ON). 111,
at which it enters the orbit. B The internal carotid nerve (arrow) crosses oculomotor nerve; V-1, ophthalmic nerve; V-2, maxillary nerve; V-3,
the inferior surface of the trigeminal ganglion and supplies branches to mandibular nerve, VI,abducens nerve. Magnification bars, 1 mm.
 NERVES FROM PTERYGOPALATINE GANGLION TO EYE 99

Fig. 4. Histological sections of nerves in the rete mirabile. A: Many A single ganglion cell is present in a very small nerve. Magnification
nerve bundles (arrowheads) are scattered through the connective tissue bars: A, 200 pm; B, 50 pm; C, 20 pm.
of the arterial rete. B: A cluster of ganglion cells lie at a nerve junction.

Fig. 5. Pathway 2: Nerves to the inferior optic nerve sheath. A: Branches

(arrows) from the nerve of the pterygoid canal (“(2) and fmm a prom-
inent accessory ganglion (open arrow) near the orbital apex extend to
the inferior surface of the optic nerve (ON). Here they turn to travel
toward the eye. Other nerves (arrowheads) accompany the interior eth-
moidal artery (IEA) fmm the orbit through the optic foramen to the
cranial cavity. B Another preparation demonstrates the ofken branching
course of nerves from the pterygopalatine ganglion on the inferior surface
of the optic nerve. 111, oculomotor nerve; CG, ciliary ganglion; SCN, short
ciliary nerve. Magnification bars, 1mm
100 T.LIN ET AL.

Fig. 6. Pathway 3 Nerves connecting with terminal branches of the

nasociliary nerve. A: Whole mount of M y dissected nerves connecting
the distal pterygopalatine ganglion (PPG) and the terminal branches of
the nasociliary nerve (NCN). These nerves (between arrows) travel me-
dially from the pterygopalatine ganglion, below and around the extra-
ocular muscle cone, and join the ethmoidal and infratrochlear nerves.
B Medial view of a partially disseded preparation. Stained nerves (ar-
rows) fromthe pterygopalatine ganglion (PPG)join the branches of the
nasociliary nerve (open arrows). Some fine stained nerves pass back
along the nasociliary nerve to reach the superior surface of the optic sheath, where it joins other nerves directed to the eye. Additional nerves
nerve (ON). NPC, nerve of the pterygoid canal. C: The nasociliary nerve (arrowhead)from the pterygopalatine ganglion are visible on the inferior
is lifted away from the superior surface of the optic nerve. A small stained optic nerve sheath. CA, ciliary artery. Magtllfication bars: A, 5 m;B,
nerve (arrows) transfers from the nasociliary nerve to the optic nerve C, 0.5 mm.

Weddell, 1959; Grimes and von Sallmann, 1960). The The pathways by which nerves from the pterygopa-
omission is not surprising, because these nerves do not latine ganglion reach the optic nerve in the cat are
stain by the silver method used as a dissection aid in circuitous and differ from those described in other
the earlier studies (Ruskell, 1965; Kuwayama et al., mammalian species. In comparison to cats, the ptery-
1987), and they are too fine to be evident in unstained gopalatine ganglia of monkeys (Ruskell, 1970a),rabbits
preparations. (Ruskell, 1965), and rats (Kuwayama et al., 1987) lie
 NERVES FROM PTERYGOPALATINE GANGLION TO EYE 101

Fig. 7. Final common pathway. Near the eye, nerves traveling from
the pterygopalatine ganglion by all three paths form a network of tine
nerves that surrounds and accomuanies the ciliary artery (CA) but is
distinct fmm its intramural innekation. All of these nerves enter the
eye with branches of the ciliary artery or &r joining ciliary nerves, Fig. 8. A, B Cross sections of representative nerves originating from
The nmbers, correspondingto those in Figure 1, indicate the pathways the PteWZOPalatine g a d i o n on the inferior surface of the optic nerve.
by which the labeled nerves reach the optic nerve. SCN,short These nerves, taken from two different eyes, contain mostly unmyeli-
nerves. Magmfkation bar, 1 mm. nated nerve fibers but also a few myelinated axons. Magnification bar,
10 um.

NasociIiar\j
nerve

Pterygopalatine

pterygoid canal

nerve
Fig. 9. Schematic diagram illustrating the nerve pathways between
Ganglion the pterygopalatine ganglion and the eye in cats. The numbering of the
cells in Rete pathways corresponds to that in Figure 1.
102 T. LIN ET AL.

closer to the cranial nerves in the orbital fissure, and Roland and Marianne E. Sargent Teaching and Re-
their orbital branches travel a relatively short distance search Fund of the Scheie Eye Institute.
to join the retro-orbital nerve plexus formed around the
cranial nerves. Nerves from the retro-orbital plexus dis- LITERATURE CITED
tribute to orbital structures along the paths taken by Christensen, K 1934 The innervation of the nasal mucosa, with special
reference to its afferent supply. Ann. Otolaryngol., 43:1066-1083.
the cranial nerves. The unusual pathways in the cat Christensen, K 1935-1936 Sympathetic and parasympathetic nerves
presumably are dictated by the position of the ganglion, in the orbit of the cat. J. Anat., 70:225-233.
well within the orbit and at a considerable distance Davis, D.D., and H.E. Story 1943 Carotid circulation in the domestic
from the entry site of the cranial nerves. cat. Publ. Field Mus., Zool. Ser., 28:l-47.
The extensive nerve plexus in the rete mirabile of the Gienc, J. 1977 The application of histochemical method in the anatom-
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- - ~- ---
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with special attention to the rete mimbik conjugaturn in the cat. J.
thetic ganglion, it contains small aggregates of ganglion Comp. Neurol., 121:305-311.
cells, and it sends some nerves to the eye. Grimes, P.A., and L. von Sallmann 1960 Comparative anatomy of the
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Uddman, R., J. Alumets, B. Ehinger, R. Hakanson, I. Loren, and F.
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