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The Architecture of the Connective Tissue in the Musculoskeletal System - An Often Overlooked Functional Parameter as to Proprioception in the Locomotor Apparatus f

The Architecture of the Connective Tissue in the Musculoskeletal System - An Often Overlooked Functional Parameter as to Proprioception in the Locomotor Apparatus f

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VAN DER WAL: CONNECTIVE TISSUE ARCHITECTURE AND PROPRIOCEPTION
1
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 NTERNATIONAL
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R E S E A R C H
The Architecture of the Connective Tissue inthe Musculoskeletal System—An OftenOverlooked Functional Parameter as toProprioception in the Locomotor Apparatus
Jaap van der Wal, MD, PhD
University Maastricht, Faculty of Health, Medicine and Life Sciences, Department of Anatomy and Embryology, Maastricht, Netherlands
 Editor’s Note:
This article is based on the doctoralthesis presented by the author at the University Maastricht in 1988: “The Organization of the Substrateof Proprioception in the Elbow Region of the Rat.”
The architecture of the connective tissue, in-cluding structures such as fasciae, sheaths, andmembranes, is more important for understand-ing functional meaning than is more traditionalanatomy, whose anatomical dissection methodneglects and denies the continuity of the con-nective tissue as integrating matrix of the body.The connective tissue anatomy and architec-ture exhibits two functional tendencies that arepresent in all areas of the body in different waysand relationships. In body cavities, the “dis-connecting” quality of shaping space enablesmobility; between organs and body parts, the“connecting” dimension enables functionalmechanical interactions. In the musculoskeletalsystem, those two features of the connectivetissue are also present. They cannot be foundby the usual analytic dissection procedures. Anarchitectural description is necessary.This article uses such a methodologic approachand gives such a description for the lateral el-bow region. The result is an alternative archi-tectural view of the anatomic substrate involvedin the transmission and conveyance of forcesover synovial joints. An architectural descrip-tion of the muscular and connective tissue or-ganized
in series
with each other to enable thetransmission of forces over these dynamic enti-ties is more appropriate than is the classicalconcept of “passive” force-guiding structuressuch as ligaments organized
in parallel
to activelyforce-transmitting structures such as muscleswith tendons.The discrimination between so-called jointreceptors and muscle receptors is an artificialdistinction when function is considered.Mechanoreceptors, also the so-called musclereceptors, are arranged in the context of forcecircumstances—that is, of the architecture of muscle and connective tissue rather than of theclassical anatomic structures such as muscle,capsules, and ligaments. In the lateral cubitalregion of the rat, a spectrum of mechanosensitivesubstrate occurs at the transitional areas betweenregular dense connective tissue layers and themuscle fascicles organized
in series
with them.This substrate exhibits features of type and loca-tion of the mechanosensitive nerve terminals thatusually are considered characteristic for “jointreceptors” as well as for “muscle receptors.”The receptors for proprioception are concen-trated in those areas where tensile stresses areconveyed over the elbow joint. Structures can-not be divided into either joint receptors ormuscle receptors when muscular and collagen-ous connective tissue structures function inseries to maintain joint integrity and stability.In vivo, those connective tissue structures arestrained during movements of the skeletalparts, those movements in turn being inducedand led by tension in muscular tissue. In prin-ciple, because of the architecture, receptors canalso be stimulated by changes in muscle ten-sion without skeletal movement, or by skeletalmovement without change in muscle tension. Amutual relationship exists between structure(and function) of the mechanoreceptors and thearchitecture of the muscular and regular denseconnective tissue. Both are instrumental in thecoding of proprioceptive information to the cen-tral nervous system.
KEYWORDS: Fascia, dissection, connective tissue,skeletal muscle, proprioception, elbow joint
PHILOSOPHIC AND METHODOLOGICINTRODUCTIONHow to Define Fasciae Anatomically, inGeneral and in the Musculoskeletal Systemin Particular?
Some thirty-five years ago, when I received my firsttraining as anatomist, it was not customary to focusone’s methodologic attention on the anatomy of 
 
VAN DER WAL: CONNECTIVE TISSUE ARCHITECTURE AND PROPRIOCEPTION
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connective tissue in general or of fasciae in particular.On the contrary, one was more or less trained to con-sider fasciae to be connective layers that had to beremoved. This approach is related to the fact that theproper method and procedure of anatomy was and stillis dissection.Although dissection is no longer the main approachin visualizing the anatomy and structure of the humanbody—modern imaging techniques can do so in the liv-ing body—”dissectional thinking” still is the mainmethod of analyzing the body in its anatomy. But in thedays of my training, one had to separate—to “dissect”—and the revealed structures had to be “cleaned” and“cleared” of connective tissue. Connective tissue wassomething resembling a covering or sleeve over andbetween the dissected structures. Therefore it often hadto be removed during the dissection procedure.Most anatomy textbooks today show muscles as dis-crete anatomic structures with the surrounding andenveloping connective tissue layers removed. Whenconnective tissue was met as a layer, a membrane, afascia covering a body structure, organ, or region, itwas given a name derived from the anatomic substratethat the layer covered. Connective tissue anatomy isoften defined as a sub-organization of anatomic struc-tures such as muscles, organs, and so on. Fasciae arethus considered to be “part of” organs and structures.In leading textbooks, fasciae are therefore definedas “masses of connective tissue large enough to bevisible with the unaided eye”
(1)
(p. 42) and classifiedas anatomic entities or structures related to organs. Butare fasciae, membranes, sheaths in the body in factdistinct and discrete anatomic structures, or are wedealing with continuity? Is the anatomical view miss-ing something when it allocates parts of this fascialcontinuity to anatomic structures and entities such asbody walls or regions (for example, fascia endo-thoracica or fascia colli media), organs (for example,fascia renalis), or body parts (for example, fascia cru-ris)? In addition, does a topographic perspective onfascia give any clue about the kind of architectural,functional–mechanical relationship being dealt with?Schleip mentions the fascia as “the dense irregularconnective tissue that surrounds and connects everymuscle, even the tiniest myofibril, and every singleorgan of the body forming continuity throughout thebody.”
(2,3)
In this way, fascia is considered an impor-tant integrative element in human posture and move-ment organization (locomotor apparatus) and is oftenreferred to as the “organ of form.”
(4)
Does an analyti-cal and “dissectional” approach to anatomy do justiceto this concept?In removing or dissecting the connective tissue inthe form of “layers,” every anatomist observes, butoften overlooks, various degrees of attachment. Some-times a layer of fascia is just loosely connected withthe underlying or neighboring structure or tissue; some-times, it is very tight and interwoven with it, and thefascia really has to be cut away, as is the case with thefascia cruris, for example. In both cases, the conceptof “dissected means discrete” tends to remain, withfascia viewed as distinct from other tissues, except forthose clearly organized in a mechanical
in-series
rela-tionship with muscular tissue, as in recognized auxil-iary structures such as tendons and aponeuroses.This methodologic mentality has also lead traditionalanatomy to dissect the musculoskeletal system intodiscrete anatomic structures as represented by bones, joints, and muscles. The present article shows that ar-chitectural and mechanical spatial relationships be-tween the various tissue components of themusculoskeletal system reveal functional units that
goacross
the traditional anatomic entities of bones, joints,and muscles.This larger view of 
functional
relationships andcoherence is supported by modern neurophysiology. Inthe central nervous system, the traditional anatomicorganization of the musculoskeletal system is only verypoorly represented topologically, if at all. The func-tional and coordinated components of position andmotion are not the muscles (and joints), but movementsand performed actions. Modern task-dependent mod-els as initiated by Loeb
(5,6)
indicate that motor unitsare not necessarily organized in the central nervoussystem with respect to individual motor nuclei, butaccording to behavioral tasks. This organization sug-gests that humans conceptualize a locomotion sys-tem in a
broader sense,
including the coordinatingand regulating nervous system (central as well as pe-ripheral), and discriminate that from the locomotionsystem in the
narrower sense
(locomotor appara-tus), which is represented by the actual musculoskel-etal system.
Continuity and Connectivity—ConnectiveTissue as Matrix
Under the procedural and mental scalpel of theanatomist, the continuity of the connective tissue ascentral matrix of the body has been lost. The pri-mary connective tissue of the body is the embryonicmesoderm. The mesoderm represents the matrix andenvironment within which the organs and structuresof the body have been differentiated and therefore areembedded. The German embryologist Blechschmidttherefore distinguished the mesoderm as germinallayer: an “inner tissue” in opposition to the ectodermand endoderm as “limiting tissues.” In histology, “lim-iting tissue” is commonly called epithelium and isconstituted almost solely of cells, with relatively lit-tle intercellular space. “Inner tissue” could be de-scribed as undifferentiated connective tissue,
mesenchyme,
and is in principle organized in threecomponents: cells, intercellular space (interstitial sub-stances), and fibers.
(7,8)
Most derivatives of the so-called inner tissue can be identified in histology asconnective tissue, including the head-mesenchyme asderivative from neurodermal tissue.
 
VAN DER WAL: CONNECTIVE TISSUE ARCHITECTURE AND PROPRIOCEPTION
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As to the
functional
development and differen-tiation of the mesenchyme, there are two patterns of “connection.”The first pattern is the development of “intercellu-lar space,” which represents a fissure functioning as asliding and slipping space as is seen in the formationof coelom (body cavities) and of joint “cavities.” Inthis pattern, spatial separation is ensured and thereforemotion is enabled. In such cavity formation processes,the primary enlarged intercellular space is lined up anddelimited by an epithelium (in body cavities, a so-calledmesothelium). Such epithelia more or less depend onthe presence of continuous motion for their functionalmaintenance. Fascial layers such as peritoneum andpleural membrane tend to adhere as soon as the move-ment of the related structures and organs becomes ab-sent. This phenomenon can also be observed inimmobilized joints, showing that, in functional perspec-tive, body cavities and joint spaces have similarities.The second pattern of development and differentia-tion of the mesenchyme is the formation of a bindingmedium, either fibers (as in regular dense connectivetissue structures such as membranes and ligaments) orinterstitial substrate and matrix (for example, configuredin cartilaginous joints). This pattern represents the func-tional tendency of “connecting” by means of the tissuecomponents of the mesenchyme (one or a combinationof cells, intercellular substance, and fibers).In such a way, a whole spectrum of connectivitycould be described in the musculoskeletal system. Onthe one extreme, connecting structures resemble the
desmal
sutures in the skull, where dense connectivetissue membranes indeed construct a nearly immobile joint connection. The other extreme is represented bythe synovial joints (articulations), where the uttermostmobility is exerted. This latter configuration is alsoshown in the fissures of the body cavities, where or-gans and body walls and organs themselves are “con-nected” in a relationship of mobility. The cartilaginous joints (symphyses) more or less represent an interme-diate scale of connecting: in humans, nearly all theclassical symphyses (such as the ones between thevertebrae or the two pubic bones) tend to the formationof an articulating fissure.One methodologic restriction has to be made: Theseconcepts are valuable only in a phenomenologic andfunctional approach. They do not tell anything aboutthe conditions affecting differentiation of these tissuesand structures. From the perspective applied here, theprimary connective tissue may “connect” (“bind”) orit may “dis-connect” (“create room”).
Gray’s Anatomy
states that “joints in principle are connections betweenbones (arthroses)” but that the “specialized connec-tive tissues of the constituted joints can be either solidor develop a cavity”
(1)
(p. 103). The synovial joints arecalled
di
arthroses. They connect in principle two
en-chondral
bones (with the mandibular and sternoclavicu-lar joints as exceptions). The non-synovial solid jointsare called
syn
arthroses. Depending on the propertiesof the “intervening” connective tissue, the latter arefibrous joints (sutures, gomphoses, and the syn-desmoses) or cartilaginous joints (synchondroses). Fi-brous joints are usually composed of regular denseconnective tissue, sometimes of somewhat more fi-broelastic connective tissue.
Connection and Disconnection—Two Typesof Fasciae
This view of two types of connectivity is also appli-cable to the anatomy of fasciae. In general, fasciae inthe musculoskeletal system exhibit two different me-chanical and functional types:
There exist muscular fasciae adjacent to spacesthat are filled with loose areolar connective tissue(“sliding tissue”) and, sometimes, adipose tissue.They enable the sliding and gliding of muscles(and tendons) against each other and against otherstructures.
There also exist intermuscular and epimysial fas-ciae that serve as areas of insertion for neighboringmuscle fibers, which, in this way, can mechani-cally reach a skeletal element via those fasciaewithout necessarily being attached directly to thebone.
(9)
In osteopathic circles, the continuum and continuityof the “connective tissue apparatus” in the human isemphasized. Such a view is in harmony with the viewdescribed here, in particular if the formation of cracksand fissures (“articulating spaces”) as a way of “con-necting” that enables mobility are considered. The prin-cipal function of mesoderm as “inner tissue” is“mediating” in the sense of “connecting” (binding) and“disconnecting” (shaping space). This multiple func-tionality is reflected in the wavering and divergent clas-sifications that are given to connective tissue intextbooks of anatomy and histology. For example,
Gray’s Anatomy
categorizes connective tissue basedon the degree of orientation of the fibrous components:irregular connective tissue (including loose areolar,dense irregular, and adipose tissue) and regular (dense)connective tissue
(1)
(p. 41). Within the first category,areolar (“loose”) connective tissue “holds” organs andepithelia “in place” and has a variety of fibers, includ-ing collagen and elastin. Regular dense connectivetissue, on the other hand, forms ligaments and tendons.Elsewhere, the book discriminates ordinary (“general”)types of connective tissue, special skeletal types (boneand cartilage), and hemolymphoid tissue as a third cat-egory
(1)
(p. 46). The first two in this category are clas-sified as “supportive connective tissue”; bone (osseoustissue) makes up virtually the entire skeleton in adultvertebrates, and in most other vertebrates, cartilage isfound primarily in joints, where it provides cushioning.The usual classifications of connective tissue, in-cluding fasciae, not based upon functional criteria are

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