Sensory Nerve Endings in the AnteriorCruciate Ligament (Lig. cruciatum

anterius) of SheepZ. HALATA,* C. WAGNER, AND K.I. BAUMANN

Department of Functional Anatomy, Institute of Anatomy, University HospitalHamburg-Eppendorf, D-20246 Hamburg, Germany

ABSTRACTThis study examines the structure of sensory nerve endings in the sheep

anterior cruciate ligament (ACL). Three types of nerve endings are found:free nerve endings (FNE), Ruffini corpuscles, and lamellated corpuscles.

The FNE (more than 100) are found subsynovially. The afferent nervefibres are either thin myelinated axons (Ad) or C fibres with diameters of 1–2µm. FNE have been reported to function as thermoreceptors and polymodalnociceptors. In addition, FNE are also seen between fascicles of collagenfibres, often close to blood vessels. Part of this group may be efferentautonomic fibres controlling local blood flow.

The corpuscles are seen subsynovially and between fascicles of connec-tive tissue close to the attachment points of the ACL. A ligament containsabout 20 Ruffini corpuscles, which are mainly located in the subsynovialconnective tissue. They consist of cylinders formed from perineural cellssurrounding the afferent myelinated axons (diameters 4–5 µm) with en-larged nerve terminals anchored between collagen fibres. These enter inbundles from the surrounding connective tissue at one open pole, passthrough the length of the cylinder, and leave at the other pole. Functionally,Ruffini corpuscles have been described as slowly adapting stretch receptors.

Lamellated corpuscles (usually between 5 and 15) are found in thesubsynovial connective tissue. The afferent myelinated axon has a diameterof 4–6 µm, and the nerve terminal is located in the centre of numerous layersformed by lamellated terminal glial cells and by a perineural capsule. Theyare known to function as rapidly adapting pressure receptors.

The most important function of the ACL is its mechanical function, butadditional sensory functions must be considered triggering reflex mecha-nisms in case of extreme positioning or overload. Anat Rec 254:13–21,1999. r 1999 Wiley-Liss, Inc.

Key words: mechanoreceptors; cruciate ligament; Ruffini corpuscle; freenerve ending; lamellated corpuscle

In traumatology, the knee joint has become a focus ofinterest. The number of sports injuries is steadily growing,causing increasing financial burden through treatmentcosts and sick leave. Especially ruptures of the anteriorcruciate ligament (ACL) and their therapy are attractingthe interest of traumatologists and orthopaedic surgeons.The concepts for the treatment of injured cruciate liga-ments are still controversial (Haus, 1996). Many authorsagree that the ligaments do not serve solely mechanicalfunctions but are ‘‘sensors’’ monitoring the position of theknee joint (Jackson, 1993; Ellaway et al., 1996). Especiallyin case of wrong positioning or overload, they can trigger

reflexes at the level of the spinal cord, adjusting the tone ofskeletal muscle (Brand, 1986; Solomonow et al., 1987;

Grant sponsor: Deutsche Forschungs Gemeinschaft; Grantnumber: Ha 1194/3-2; Grant sponsor: Verein zur Forderung derErforschung und Bekamfung rheumatischer Erkrankungen, BadBramstedt e. V.

*Correspondence to: Zdenek Halata, Department of FunctionalAnatomy, University of Hamburg, UKE, Martinistr. 52, D-20246Hamburg, Germany. Fax: 149 40 4717 2845.E-mail: kbaumann@uke.uni-hamburg.de

Received: 23 April 1998; Accepted: 7 July 1998

THE ANATOMICAL RECORD 254:13–21 (1999)

r 1999 WILEY-LISS, INC.

Johansson et al., 1991a). The present study investigatesthe structure and distribution of mechanoreceptors andtheir innervation in the ACL using light and electronmicroscopy.

The presence of nerve endings in the human ACL wasfirst reported by Schultz et al. (1984) and later by Zimny etal. (1986) and Schutte et al. (1987) based on light micro-scopic evidence. The first detailed electron microscopicfindings of sensory nerve endings in the ACL were pub-lished by Halata and Haus (1989). Electrophysiologicalrecordings from ACL receptors during movements of theknee joint were made by Krauspe et al. (1992).

In order to optimise the therapy of ACL injuries, animalexperimental studies are needed. However, small animalsare known to have only very few corpuscular mechanore-ceptors in the cruciate ligaments (Marinozzi et al., 1991).In contrast, sheep are highly suited for such experimentalprocedures. The knee joint is easily accessible, and theanatomical situation is rather similar to that in man. Thisstudy is the first detailed electron microscopical investiga-tion of nerve endings and mechanoreceptors in the ACL ofsheep. Preliminary results have been published in ab-stract form (Halata and Wagner, 1995).

MATERIALS AND METHODSWith the approval of the animal research ethics commit-

tee of the University of Hamburg, the anterior cruciateligaments of sheep were investigated using light andelectron microscopy. Five adult sheep were sacrificed withT61t (Hoechst, Frankfort, Germany) (a mixture of pento-barbital, d-tubocourarin, and a local anaesthetic made byHoechst). The knee joints of both legs were injected with6% glutardialdehyde for in situ fixation prior to surgicalremoval of the ligaments. Then the ligaments were dividedinto proximal (femoral) and distal (tibial) halves andplaced in 6% glutardialdehyde at 4°C for 20 min. Thehalves were cut into 5 mm thick slices and kept in the samesolution for several hours. Postfixation was carried outwith 1 % OsO4 in 0.1 M buffer. Several dozen tissue blockswere obtained from each sheep.

After dehydration in increasing concentrations of etha-nol, the samples were embedded in glycidether. Semithinsections were stained according to Laczko et al. (1975).Appropriate sections were reimbedded for ultrathin section-ing and contrasted with uranyl acetate and lead citrate(Reynolds, 1963). The electron microscope was a Philips200 (Philips, The Netherlands).

RESULTSThe anterior face of the ACL is covered with synovial

membrane. Branches of the posterior articular nerve(PAN) originating from the tibial nerve innervate bothcruciate ligaments. Thin branches of the nerve follow bloodvessels through the loose connective tissue, penetrate thecapsule, and then run between the ligaments. They con-tain myelinated and unmyelinated axons with diametersof 2–10 µm and about 1 µm, respectively.

Three types of sensory nerve endings were found in theACL of sheep: free nerve endings (FNE), Ruffini cor-puscles, and small lamellated corpuscles.

Free Nerve Endings (FNE)FNE are terminals of nonmyelinated axons and/or thin

myelinated Ad fibres. In the ACL, they are found in large

numbers below the synovia (Fig. 1). In addition, they canbe seen in the connective tissue between collagen fibres,often close to small blood vessels. Their total number isestimated to be more than 100 per cruciate ligament.About half of the total number is found in the proximalthird of the ligaments. The distal third is less denselyinnervated, with even lower numbers in the middle third.The thin myelinated Ad fibres have diameters of 1–2 µmand branch into several unmyelinated parts ending withterminal enlargements. Most of the axolemma of theterminals is covered only by the basal lamina but in someparts also cytoplasmic processes of Schwann cells are seenadjacent to the terminals (Fig. 1). Within the axoplasm,groups of mitochondria and clear vesicles (diameter about600 nm) are frequently seen. The nerve terminals of thenonmyelinated C fibres have similar structures.

Ruffini CorpusclesRuffini corpuscles are mainly seen subsynovially in the

stratum fibrosum of the ACL (Fig. 2). Their total numberwas about 20 per ligament. Again, they are concentrated inthe proximal parts. However, a particularly large varietyinterspersed between the collagen bundles of the ligamentis seen in small numbers in the distal third.

Ruffini corpuscles consist of cylinders formed from lay-ers of perineural cells with open poles on both ends.Collagen fibres from the surrounding tissue enter andleave the cylinder at these ends, passing through thelength of the cylinder core. Each corpuscle is supplied by amyelinated axon of about 5 µm diameter (Fig. 4). The axonenters the corpuscle at the long side of the cylinder, wherethe perineurium merges with the capsule. Within thecylinder, the axon branches into several unmyelinatedfibres with enlarged terminals containing groups of mito-chondria and empty vesicles. These terminals are an-chored between the bundles of collagen fibres, often withfinger-like protrusions containing clear vesicles (Fig. 4).Two to five layers form the cylinder’s capsule. Each layerconsists of flat perineural cells, covered on the outside bybasal laminae. Collagen fibres run between adjacent basallaminae. The ends of the cylinders are often narrower,giving the cylinder a spindle-like shape.

In contrast, in the femoral third of the ACL of sheep wefound on average, spread out between the bundles ofcollagen fibres, three large Ruffini corpuscles consisting ofone cylinder each. They are about 600 µm long, 100 µm indiameter, and similar in structure to Golgi tendon organs(Figs. 3, 6). The perineural capsule has five flat layers ofcells. The cylinders are open at both ends, where thecapsule is lacking completely and bundles of collagenfibres from the ligament enter or leave the cylinder. Theyare supplied by myelinated axons of about 6 µm diameter.After entering the cylinder at the long side, the axon losesits myelination and branches into nerve terminals anchor-ing between bundles of collagen fibres. The ultrastructureof the nerve terminals, the bundles of collagen fibres, andthe perineural capsule (Fig. 5) are rather similar to thesmaller Ruffini corpuscles. Their appearance resemblesGolgi tendon organs apart from the fact that they arelocated in a ligament rather than in a tendon. Theseintrafascicular Ruffini corpuscles contain a thick subcapsu-lar space (about 15 µm) filled with amorphous substance,sparse collagen fibres, and some flat fibroblasts. In con-trast, such a thick subcapsular space is not seen in Ruffinicorpuscles located subsynovially.

14 HALATA ET AL.

Lamellated CorpusclesLamellated corpuscles (Figs. 6–8) are found between

bundles of collagen fibres mostly in the proximal part ofthe ACL. Their total number is between 5 and 15. They areabout 100 µm long and 20–40 µm in diameter, consisting ofone or two inner cores embedded into amorphous materialand surrounded by a multilayered perineural capsule. Insome cases the corpuscles share a common capsule with anintrafascicular Ruffini corpuscle (Fig. 6). Each lamellatedcorpuscle is supplied by one myelinated axon with adiameter of 4–6 µm. After losing its myelin sheath, usuallyone or occasionally two nerve terminals are formed, cov-ered by five to ten cytoplasmic laminae (each about 2 µmthick) of the terminal Schwann cell. The enlarged nerveterminal located in the middle of the inner core containsmitochondria and electron-microscopically clear vesicles(Fig. 7).

Attachment plaques are often seen between the axo-lemma and innermost layer of the terminal Schwann cellsas well as between lamellae of inner core cells (Fig. 8).Spiny protrusions extend from the axolemma and axo-

plasm into the space between the cytoplasmic lamellaefrom the Schwann cells. Empty vesicles are often seen inthe axoplasm of these protrusions. The space between theinner core and the capsule is often filled with amorphoussubstance, sparse collagen fibres, and fibroblasts. Betweenthe lamellae and the capsule is a small subcapsular space,sometimes containing fibroblasts. When several nerveterminals are found, they all originate from a singlemyelinated axon.

DISCUSSIONMacroscopically, the innervation of the sheep’s knee

joint and its ligaments has been investigated by Lorke etal. (1993) and found to be very similar to the situation inman (Jeletzky, 1930; Gardner, 1944; Haus, 1996). Themain nerve supplying the cruciate ligament is the poste-rior articular nerve (PAN) derived from the tibial nerve. Inman, this nerve is reported to have sometimes two or threebranches (Gardner, 1944), which is rarely seen in sheep(Lorke et al., 1993). Usually branches of the nerve accom-pany arteries of the joint capsule and cruciate ligaments.

Fig. 1. Electron micrograph of a free nerve ending (FNE) in the anterior aspect of the sheep ACL in crosssection. The nerve terminal (N) contains several mitochondria and neurotubules. It is incompletely covered byprocesses of a Schwann cell (S) and basal lamina. Fibroblasts (F) send flat processes between bundles ofcollagen fibres.

15NERVE ENDINGS IN CRUCIATE LIGAMENTS

In man, the nerve forms a meandering network (Haus,1996).

All three types of sensory nerve endings found inmammalian joint capsules (Polacek, 1966) were also seenin the ACL (i.e., free nerve endings, Ruffini corpuscles, andlamellated corpuscles). Thus, in terms of sensory innerva-tion, the sheep cruciate ligament and joint capsule aresimilarly equipped. In contrast, in the capsule and liga-ments of the knee joint in rat, lamellated corpuscles arenot regularly found (Marinozzi et al. 1991).

The structure of free nerve endings resembles thatdescribed in the joint capsule of the cat by Heppelmann etal. (1995). Under the electron microscope, one can differen-tiate afferent nonmyelinated nerve fibres located close tothe blood vessels from efferent autonomic nerves supply-ing the vascular smooth muscle only when one gets a clearimage of the nerve terminal. Physiologically, afferent freenerve endings are believed to be mainly involved in theperception of pain (Heppelmann et al., 1995; Krauspe etal., 1992). In addition, free nerve endings in variouslocations are known to act as high-threshold mechanorecep-tors responding to strong mechanical stimuli (Andres etal., 1985; Khalsa et al., 1997). In the skin, free nerveendings can also serve as thermoreceptors (Hensel, 1973)and function as polymodal nociceptors (Kruger et al., 1981;

Kruger and Halata, 1996). The large number of free nerveendings in the cruciate ligaments suggests that many ofthose from afferent fibres have nociceptive or high-threshold mechanoreceptive functions. Furthermore, arich supply with efferent nonmyelinated fibres serving theneural control of local blood flow is well documented(Ferrell et al., 1993; McDougall et al., 1997).

Ruffini corpuscles are known to be slowly adaptingstretch receptors (Chambers et al., 1972). The structure ofboth large and small corpuscles is optimally designed for

Fig. 4. Electron microscopic close-up of the larger cylinder of theRuffini corpuscle shown in the semi-thin section of figure 2. Nerveterminals (N) packed with mitochondria and surrounded by flat Schwanncells (S) are squeezed between bundles of collagen fibres. In some areasfinger like protrusions (=) not covered by Schwann cells and filled withclear vesicles extend from the nerve terminal.

Fig. 5. Electron micrograph showing the cross section of a bundle ofseveral nerve terminals of a Ruffini corpuscle surrounded by a flatfibroblast (F). The nerve terminals (N) are squeezed between bundles ofcollagen fibres. Together with flat processes of terminal Schwann cellsthey divide the bundles into several compartments. Amorphous sub-stance with sparse collagen fibres is seen between the bundle ofterminals and the capsule of the Ruffini corpuscle formed by severallayers of flat perineural cells (P).

Fig. 2. Semi-thin cross section of the subsynovial layer of sheep ACLshowing two Ruffini corpuscles (R) consisting of two cylinders of perineu-ral cells and a plexus of capillaries between them. Each cylinder issupplied by a single myelinated axon (=) and surrounded by a capsule ofseveral layers of flat perineural cells. A close-up is given in Figure 4.

Fig. 3. Semi-thin section of an intrafascicular Ruffini corpuscle. Onecylinder contains one myelinated axon (=) branching into several nerveterminals. A close-up is given in Figure 5.

16 HALATA ET AL.

Figures 4 and 5.

17NERVE ENDINGS IN CRUCIATE LIGAMENTS

this function (Grigg and Hoffmann, 1984). The wall of thecylinder is often incomplete, allowing bundles of collagenfibres to enter the corpuscle also at the long side of thecylinder. It is assumed that tension is transmitted viacollagen fibres to the nerve terminal or its finger-likeprotrusions, causing small deformations and resulting inthe generation of action potentials. Differences arise fromthe structure and texture of the connective tissue. In theloose connective tissue of the stratum fibrosum, the Ruffinicorpuscles are small, and the capsules of the cylinders areoften incomplete. In well-organised connective tissue, theform of the cylinders becomes clearer, the perineuralcapsule is more complete, and the number of layers of theperineural capsule increases (Halata, 1988). The liga-ments in the capsule of the knee joint in primates (Halataet al., 1984) as well as the human ACL (Halata and Haus,1989) contain similar corpuscles. Large Ruffini corpusclesresembling Golgi tendon organs were also found in theoblique popliteal ligament of the canine joint capsule

(Schenk et al., 1996). Very large Ruffini corpuscles in thecruciate ligaments are often referred to as Golgi tendonorgans (Zimny et al., 1986; Schutte et al., 1987). However,we feel this term should be reserved for those complexmechanoreceptors at the transition between muscle andtendon (Schoultz and Swett, 1972).

Lamellated corpuscles (e.g., Pacinian corpuscles in thesubcutaneous tissue) function as low-threshold, rapidlyadapting mechanoreceptors (Grigg, 1975). Their structureis similar to those lamellated corpuscles found in the jointcapsule or synovia of other larger mammalian species thatwere investigated electron-microscopically: cat (Halata,1977), monkey (Halata et al., 1984), man (Halata et al., 1985,Halata and Haus, 1989), and dog (Schenk et al., 1996). Inolder, light-microscopic studies, such corpuscles were de-scribed as Golgi-Mazoni corpuscles (Polacek, 1966). However,the ultrastructure as examined by electron microscopy isbasically the same as in the other lamellated corpuscles.We saw in several blocks lamellated corpuscles in close

Fig. 6. Low magnification electron micrograph of 2 mechanoreceptorcorpuscles from sheep ACL. The Ruffini corpuscle (R) consisting of abundle of nerve terminals and surrounded by a thin layer of a fibroblast (F)is embedded in amorphous material and surrounded by a capsule (C).Adjacent is a lamellated corpuscle (L) with 2 inner cores (=) each

containing a nerve terminal (for greater detail see Fig. 7). Each corpusclehas its own capsule of perineural cells. An additional capsule (P)surrounds both corpuscles, the myelinated axon (A) supplying thelamellated corpuscle (seen in serial sections) and several capillaries.

18 HALATA ET AL.

vicinity to Ruffini corpuscles sharing a common capsule.But a separate myelinated axon rather than a branch ofthe one supplying the Ruffini corpuscle innervated theselamellated corpuscles. Both axons originate from the samenerve (PAN), so it is not surprising that a common capsulein addition to the capsules of the individual corpusclessurrounds such a conglomerate. However, this commoncapsule does not cover the entire complex but only itsproximal part. It is well possible that such a combinedcorpuscle acts as both a slowly and rapidly adaptingreceptor at the same location within the same perineuralcapsule.

Our results show that the ACL is well supplied withsensory nerve endings. It had been suggested that thecruciate ligaments do not only have mechanical functionsbut also play a sensory role in reflex control within thespinal cord, adjusting the tone of thigh muscles via g-mo-torneurones (Ellaway et al., 1996; Johansson et al., 1991b).Electrophysiological recordings from mechanoreceptors inthe ACL of cats by Krauspe et al. (1992) strongly support

this notion. The knee joint could be stabilised especially byadjusting the ischiocrural muscles through reflex mecha-nisms, as reported by Solomonow et al. (1987). However,other reports suggest that receptors in the joint capsuleplay a more important role in adjusting muscle tone, whilethose in the cruciate ligaments may come into play only inextreme situations (Khalsa and Grigg, 1997).

Surgical treatment of ruptured ACL obviously focuseson the mechanical function of the ACL. It is very likely thatthe mechanoreceptors in the distal part of the ACL losetheir nerve supply, resulting in degeneration of the recep-tors. Lamellated mechanoreceptors can be successfullyreinnervated after nerve crush under conditions allowingthe sprouting nerve fibres to grow along the guidingstructures of the distal part of the nerve (Zelena andZacharova, 1997). For reinnervation of transplanted tissueto occur, it would be essential that the nerve is carefullysutured, not just the ligament (Zelena, 1994). This istechnically not feasible and would complicate surgerytremendously. Recently, successful reinnervation of mecha-

Fig. 7. Detail of the inner core of a lamellated corpuscle with 2 nerveterminals. The nerve terminals contain mitochondria, clear vesicles,neurotubules and neurofilaments. Attachment plaques (=) with the

adjacent lamellae of the inner core are seen in several places. Theselamellae are formed by terminal Schwann cells and show cross-sectionedcollagen fibres between them.

19NERVE ENDINGS IN CRUCIATE LIGAMENTS

noreceptors in transplanted ACL without special effort tosuture the nerve has been reported (Fromm and Kummer,1994; Goertzen et al., 1994). In such cases, one may expectefferent autonomic nerve fibres to enter the graft with theblood vessels. Thus, the presence of nerve fibres in thegraft is not sufficient evidence to argue that these functionas mechanoreceptors. In our opinion, this can be confirmedbeyond doubt only by electron microscopy. Immunohisto-chemistry as carried out by Fromm et al. (1994) cannotclearly identify reinnervation of lamellated mechanorecep-tor corpuscles in graft tissue. The only report known to ususing electron microscopy (Goertzen et al., 1994) had to beretracted by the editors of the journal after thoroughinvestigations (Fulford, 1997; Abbott, 1997).

In contrast, one can expect the mechanoreceptors proxi-mal to the rupture to remain innervated and thus function-ally intact. During surgery, it should be carefully consid-ered to keep the remaining synovia and the rest of thefemoral parts of the ligament in place in order to preservesome of the sensory functions of the ligament whileotherwise concentrating on stable insertion of the trans-plant.

ACKNOWLEDGMENTSThe authors thank Ms. B. Knuts, Ms. B. Lucht, Mr. St.

Schillemeit, and Dr. A. Spaethe for excellent technicalassistance.

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