The Architecture of the

Connective Tissue in the

Musculoskeletal SystemAn
Often Overlooked Functional
Parameter as to Proprioception
in the Locomotor Apparatus
Jaap van der al! M"! Ph"
University Maastricht, Faculty of Health, Medicine and Life Sciences, Department of Anatomy and
Embryology, Maastricht, etherlands

Editor's Note: !his article is based on the doctoral thesis presented by the author at the
University Maastricht in "#$$% &!he 'rgani(ation of the Substrate of )roprioception in the Elbo*
+egion of the +at,&

The architecture of the connective tissue! includin# structures such as fasciae! sheaths!
and mem$ranes! is more important for understandin# functional meanin# than is more
traditional anatomy! %hose anatomical dissection method ne#lects and denies the
continuity of the connective tissue as inte#ratin# matri& of the $ody'
The connective tissue anatomy and architecture e&hi$its t%o functional tendencies that
are present in all areas of the $ody in different %ays and relationships' (n $ody cavities!
the )disconnectin#) *uality of shapin# space ena$les mo$ility+ $et%een or#ans and $ody
parts! the )connectin#) dimension ena$les functional mechanical interactions' (n the
musculoskeletal system! those t%o features of the connective tissue are also present'
They cannot $e found $y the usual analytic dissection procedures' An architectural
description is necessary'
This article uses such a methodolo#ic approach and #ives such a description for the
lateral el$o% re#ion' The result is an alternative architectural vie% of the anatomic
su$strate involved in the transmission and conveyance of forces over synovial ,oints' An
architectural description of the muscular and connective tissue or#ani-edin series %ith
each other to ena$le the transmission of forces over these dynamic entities is more
appropriate than is the classical concept of )passive) force.#uidin# structures such as
li#aments or#ani-ed in parallel to actively force.transmittin# structures such as muscles
%ith tendons'
The discrimination $et%een so.called ,oint receptors and muscle receptors is an
artificial distinction %hen function is considered' Mechanoreceptors! also the so.called
muscle receptors! are arran#ed in the conte&t of force circumstancesthat is! of the
architecture of muscle and connective tissue rather than of the classical anatomic
structures such as muscle! capsules! and li#aments' (n the lateral cu$ital re#ion of the
rat! a spectrum of mechanosensitive su$strate occurs at the transitional areas $et%een
re#ular dense connective tissue layers and the muscle fascicles or#ani-ed in series %ith
them' This su$strate e&hi$its features of type and location of the mechanosensitive
nerve terminals that usually are considered characteristic for ),oint receptors) as %ell
as for )muscle receptors')
The receptors for proprioception are concentrated in those areas %here tensile stresses
are conveyed over the el$o% ,oint' Structures cannot $e divided into either ,oint
receptors or muscle receptors %hen muscular and colla#enous connective tissue
structures function in series to maintain ,oint inte#rity and sta$ility' (n vivo! those
connective tissue structures are strained durin# movements of the skeletal parts! those
movements in turn $ein# induced and led $y tension in muscular tissue' (n principle!
$ecause of the architecture! receptors can also $e stimulated $y chan#es in muscle
tension %ithout skeletal movement! or $y skeletal movement %ithout chan#e in muscle
tension' A mutual relationship e&ists $et%een structure /and function0 of the
mechanoreceptors and the architecture of the muscular and re#ular dense connective
tissue' 1oth are instrumental in the codin# of proprioceptive information to the central
nervous system'
KEYWORDS: Fascia, dissection, connective tissue, skeletal muscle, proprioception, elbow oint

PHILOSOPHIC AND METHODOLOGIC
INTRODUCTION
How to Define Fasciae Anatomically in Gene!al an" in t#e M$sc$los%eletal
System in Pa!tic$la!&
Some t!irt"#$ive "ears a%o, w!en & received m" $irst trainin% as anatomist, it was not customar" to
$ocus one's met!odolo%ic attention on t!e anatom" o$ connective tissue in %eneral or o$ $asciae in
particular( On t!e contrar", one was more or less trained to consider $asciae to be connective
la"ers t!at !ad to be removed( )!is approac! is related to t!e $act t!at t!e proper met!od and
procedure o$ anatom" was and still is dissection(
*lt!ou%! dissection is no lon%er t!e main approac! in visuali+in% t!e anatom" and structure o$ t!e
!uman bod",modern ima%in% tec!ni-ues can do so in t!e livin% bod",.dissectional t!inkin%. still
is t!e main met!od o$ anal"+in% t!e bod" in its anatom"( /ut in t!e da"s o$ m" trainin%, one !ad
to separate,to .dissect., and t!e revealed structures !ad to be .cleaned. and .cleared. o$
connective tissue( 0onnective tissue was somet!in% resemblin% a coverin% or sleeve over and
between t!e dissected structures( )!ere$ore it o$ten !ad to be removed durin% t!e dissection
procedure(
1ost anatom" te2tbooks toda" s!ow muscles as discrete anatomic structures wit! t!e surroundin%
and envelopin% connective tissue la"ers removed( W!en connective tissue was met as a la"er, a
membrane, a $ascia coverin% a bod" structure, or%an, or re%ion, it was %iven a name derived $rom
t!e anatomic substrate t!at t!e la"er covered( 0onnective tissue anatom" is o$ten de$ined as a
sub#or%ani+ation o$ anatomic structures suc! as muscles, or%ans, and so on( Fasciae are t!us
considered to be .part o$. or%ans and structures(
&n leadin% te2tbooks, $asciae are t!ere$ore de$ined as .masses o$ connective tissue lar%e enou%!
to be visible wit! t!e unaided e"e.
345
3p( 675 and classi$ied as anatomic entities or structures
related to or%ans( /ut are $asciae, membranes, s!eat!s in t!e bod" in $act distinct and discrete
anatomic structures, or are we dealin% wit! continuit"8 &s t!e anatomical view missin% somet!in%
w!en it allocates parts o$ t!is $ascial continuit" to anatomic structures and entities suc! as bod"
walls or re%ions 3$or e2ample, $ascia endot!oracica or $ascia colli media5, or%ans 3$or e2ample,
$ascia renalis5, or bod" parts 3$or e2ample, $ascia cruris58 &n addition, does a topo%rap!ic
perspective on $ascia %ive an" clue about t!e kind o$ arc!itectural, $unctional9mec!anical
relations!ip bein% dealt wit!8
Sc!leip mentions t!e $ascia as .t!e dense irre%ular connective tissue t!at surrounds and connects
ever" muscle, even t!e tiniest m"o$ibril, and ever" sin%le or%an o$ t!e bod" $ormin% continuit"
t!rou%!out t!e bod"(.
37,:5
&n t!is wa", $ascia is considered an important inte%rative element in
!uman posture and movement or%ani+ation 3locomotor apparatus5 and is o$ten re$erred to as t!e
.or%an o$ $orm(.
365
Does an anal"tical and .dissectional. approac! to anatom" do ustice to t!is
concept8
&n removin% or dissectin% t!e connective tissue in t!e $orm o$ .la"ers,. ever" anatomist observes,
but o$ten overlooks, various de%rees o$ attac!ment( Sometimes a la"er o$ $ascia is ust loosel"
connected wit! t!e underl"in% or nei%!borin% structure or tissue; sometimes, it is ver" ti%!t and
interwoven wit! it, and t!e $ascia reall" !as to be cut awa", as is t!e case wit! t!e $ascia cruris,
$or e2ample( &n bot! cases, t!e concept o$ .dissected means discrete. tends to remain, wit! $ascia
viewed as distinct $rom ot!er tissues, e2cept $or t!ose clearl" or%ani+ed in a mec!anical in-
series relations!ip wit! muscular tissue, as in reco%ni+ed au2iliar" structures suc! as tendons and
aponeuroses(
)!is met!odolo%ic mentalit" !as also lead traditional anatom" to dissect t!e musculoskeletal
s"stem into discrete anatomic structures as represented b" bones, oints, and muscles( )!e
present article s!ows t!at arc!itectural and mec!anical spatial relations!ips between t!e various
tissue components o$ t!e musculoskeletal s"stem reveal $unctional units t!at %o across t!e
traditional anatomic entities o$ bones, oints, and muscles(
)!is lar%er view o$ functional relations!ips and co!erence is supported b" modern
neurop!"siolo%"( &n t!e central nervous s"stem, t!e traditional anatomic or%ani+ation o$ t!e
musculoskeletal s"stem is onl" ver" poorl" represented topolo%icall", i$ at all( )!e $unctional and
coordinated components o$ position and motion are not t!e muscles 3and oints5, but movements
and per$ormed actions( 1odern task#dependent models as initiated b" <oeb
3=,>5
indicate t!at motor
units are not necessaril" or%ani+ed in t!e central nervous s"stem wit! respect to individual motor
nuclei, but accordin% to be!avioral tasks( )!is or%ani+ation su%%ests t!at !umans conceptuali+e a
locomotion s"stem in a $roader sense, includin% t!e coordinatin% and re%ulatin% nervous s"stem
3central as well as perip!eral5, and discriminate t!at $rom t!e locomotion s"stem in t!enarro%er
sense 3locomotor apparatus5, w!ic! is represented b" t!e actual musculoskeletal s"stem(
Contin$ity an" Connecti'ity(Connecti'e Tiss$e as Mat!i)
?nder t!e procedural and mental scalpel o$ t!e anatomist, t!e continuit" o$ t!e connective tissue
as central matri2 o$ t!e bod" !as been lost( )!e primar" connective tissue o$ t!e bod" is t!e
embr"onic mesoderm( )!e mesoderm represents t!e matri2 and environment wit!in w!ic! t!e
or%ans and structures o$ t!e bod" !ave been di$$erentiated and t!ere$ore are embedded( )!e
@erman embr"olo%ist /lec!sc!midt t!ere$ore distin%uis!ed t!e mesoderm as %erminal la"er: an
.inner tissue. in opposition to t!e ectoderm and endoderm as .limitin% tissues(. &n !istolo%",
.limitin% tissue. is commonl" called epit!elium and is constituted almost solel" o$ cells, wit!
relativel" little intercellular space( .&nner tissue. could be described as undi$$erentiated connective
tissue, mesenchyme, and is in principle or%ani+ed in t!ree components: cells, intercellular space
3interstitial substances5, and $ibers(
3A,B5
1ost derivatives o$ t!e so#called inner tissue can be
identi$ied in !istolo%" as connective tissue, includin% t!e !ead#mesenc!"me as derivative $rom
neurodermal tissue(
*s to t!e functional development and di$$erentiation o$ t!e mesenc!"me, t!ere are two patterns
o$ .connection(.
)!e $irst pattern is t!e development o$ .intercellular space,. w!ic! represents a $issure $unctionin%
as a slidin% and slippin% space as is seen in t!e $ormation o$ coelom 3bod" cavities5 and o$ oint
.cavities(. &n t!is pattern, spatial separation is ensured and t!ere$ore motion is enabled( &n suc!
cavit" $ormation processes, t!e primar" enlar%ed intercellular space is lined up and delimited b"
an epit!elium 3in bod" cavities, a so#called mesot!elium5( Suc! epit!elia more or less depend on
t!e presence o$ continuous motion $or t!eir $unctional maintenance( Fascial la"ers suc! as
peritoneum and pleural membrane tend to ad!ere as soon as t!e movement o$ t!e related
structures and or%ans becomes absent( )!is p!enomenon can also be observed in immobili+ed
oints, s!owin% t!at, in $unctional perspective, bod" cavities and oint spaces !ave similarities(
)!e second pattern o$ development and di$$erentiation o$ t!e mesenc!"me is t!e $ormation o$ a
bindin% medium, eit!er $ibers 3as in re%ular dense connective tissue structures suc! as
membranes and li%aments5 or interstitial substrate and matri2 3$or e2ample, con$i%ured in
cartila%inous oints5( )!is pattern represents t!e $unctional tendenc" o$ .connectin%. b" means o$
t!e tissue components o$ t!e mesenc!"me 3one or a combination o$ cells, intercellular substance,
and $ibers5(
&n suc! a wa", a w!ole spectrum o$ connectivit" could be described in t!e musculoskeletal s"stem(
On t!e one e2treme, connectin% structures resemble t!e desmal sutures in t!e skull, w!ere dense
connective tissue membranes indeed construct a nearl" immobile oint connection( )!e ot!er
e2treme is represented b" t!e s"novial oints 3articulations5, w!ere t!e uttermost mobilit" is
e2erted( )!is latter con$i%uration is also s!own in t!e $issures o$ t!e bod" cavities, w!ere or%ans
and bod" walls and or%ans t!emselves are .connected. in a relations!ip o$ mobilit"( )!e
cartila%inous oints 3s"mp!"ses5 more or less represent an intermediate scale o$ connectin%: in
!umans, nearl" all t!e classical s"mp!"ses 3suc! as t!e ones between t!e vertebrae or t!e two
pubic bones5 tend to t!e $ormation o$ an articulatin% $issure(
One met!odolo%ic restriction !as to be made: )!ese concepts are valuable onl" in a
p!enomenolo%ic and $unctional approac!( )!e" do not tell an"t!in% about t!e conditions a$$ectin%
di$$erentiation o$ t!ese tissues and structures( From t!e perspective applied !ere, t!e primar"
connective tissue ma" .connect. 3.bind.5 or it ma" .dis#connect. 3.create room.5( .ray/s
Anatomy states t!at .oints in principle are connections between bones 3art!roses5. but t!at t!e
.speciali+ed connective tissues o$ t!e constituted oints can be eit!er solid or develop a
cavit".
345
3p( 4C:5( )!e s"novial oints are called diart!roses( )!e" connect in principle
twoenchondral bones 3wit! t!e mandibular and sternoclavicular oints as e2ceptions5( )!e non#
s"novial solid oints are called s"nart!roses( Dependin% on t!e properties o$ t!e .intervenin%.
connective tissue, t!e latter are $ibrous oints 3sutures, %omp!oses, and t!e s"ndesmoses5 or
cartila%inous oints 3s"nc!ondroses5( Fibrous oints are usuall" composed o$ re%ular dense
connective tissue, sometimes o$ somew!at more $ibroelastic connective tissue(
Connection an" Disconnection(Two Ty*es of Fasciae
)!is view o$ two t"pes o$ connectivit" is also applicable to t!e anatom" o$ $asciae( &n %eneral,
$asciae in t!e musculoskeletal s"stem e2!ibit two di$$erent mec!anical and $unctional t"pes:

)!ere e2ist muscular $asciae adacent to spaces t!at are $illed wit! loose areolar
connective tissue 3.slidin% tissue.5 and, sometimes, adipose tissue( )!e" enable t!e slidin% and
%lidin% o$ muscles 3and tendons5 a%ainst eac! ot!er and a%ainst ot!er structures(

)!ere also e2ist intermuscular and epim"sial $asciae t!at serve as areas o$ insertion $or
nei%!borin% muscle $ibers, w!ic!, in t!is wa", can mec!anicall" reac! a skeletal element via t!ose
$asciae wit!out necessaril" bein% attac!ed directl" to t!e bone(
3D5
&n osteopat!ic circles, t!e continuum and continuit" o$ t!e .connective tissue apparatus. in t!e
!uman is emp!asi+ed( Suc! a view is in !armon" wit! t!e view described !ere, in particular i$ t!e
$ormation o$ cracks and $issures 3.articulatin% spaces.5 as a wa" o$ .connectin%. t!at enables
mobilit" are considered( )!e principal $unction o$ mesoderm as .inner tissue. is .mediatin%. in t!e
sense o$ .connectin%. 3bindin%5 and .disconnectin%. 3s!apin% space5( )!is multiple $unctionalit" is
re$lected in t!e waverin% and diver%ent classi$ications t!at are %iven to connective tissue in
te2tbooks o$ anatom" and !istolo%"( For e2ample, .ray/s Anatomy cate%ori+es connective tissue
based on t!e de%ree o$ orientation o$ t!e $ibrous components: irre%ular connective tissue
3includin% loose areolar, dense irre%ular, and adipose tissue5 and re%ular 3dense5 connective
tissue
345
3p( 645( Wit!in t!e $irst cate%or", areolar 3.loose.5 connective tissue .!olds. or%ans and
epit!elia .in place. and !as a variet" o$ $ibers, includin% colla%en and elastin( Re%ular dense
connective tissue, on t!e ot!er !and, $orms li%aments and tendons( Elsew!ere, t!e book
discriminates ordinar" 3.%eneral.5 t"pes o$ connective tissue, special skeletal t"pes 3bone and
cartila%e5, and !emol"mp!oid tissue as a t!ird cate%or"
345
3p( 6>5( )!e $irst two in t!is cate%or"
are classi$ied as .supportive connective tissue.; bone 3osseous tissue5 makes up virtuall" t!e
entire skeleton in adult vertebrates, and in most ot!er vertebrates, cartila%e is $ound primaril" in
oints, w!ere it provides cus!ionin%(
)!e usual classi$ications o$ connective tissue, includin% $asciae, not based upon $unctional criteria
are not ver" consistent in t!eir cate%ories( .ray/s Anatomy de$ines $asciae as .masses o$
connective tissue lar%e enou%! to be visible wit! t!e unaided e"e.
345
3p( 675( *s e2amples o$
$ascia, t!e s!eat!s around nerves and vessels are mentioned, as are t!e $asciae .on t!e sur$ace.
o$ muscles and or%ans and between movable muscles, meant as .mec!anical isolation(. .ray/s
Anatomy makes special re$erence to t!e superficial fascia and to t!e deep fascia, t!e latter in
particular developed in limbs w!ere it condenses to t!icker nonelastic s!eat!s and cases around
t!e muscles( )!e discrete anatomic structure 3$or instance, muscle5 is considered as re$erence,
and t!ere$ore t!e $ascia is de$ined as a kind o$ secondar" au2iliar" envelope to t!at 3primar"5
structure( )!is view o$ $asciae as a kind o$ secondar" structure actuall" results $rom t!e scalpel o$
anatomists, w!o, w!ile cleanin% muscles $rom t!e $ascial la"ers, !ave disrupted anatomic
continuit" w!ere it e2ists in vivo(

CONNECTI+E TISSUE IN THE
MUSCULOS,ELETAL S-STEM. T/O
FUNCTIONAL APPEARANCES
Not Only Anatomy 0$t Also A!c#itect$!e
&n principle, onl" two kinds o$ $orces !ave to be transmitted over s"novial oints between t!e
articulatin% elements in t!e locomotor apparatus: $orces o$ compression and o$ tension(
0ompression $orces between t!e articulatin% elements are transmitted via t!e articular sur$aces o$
t!e adacent bone elements( )!e tractive $orces and mec!anical stresses over t!e s"novial oints
are assumed to be transmitted bot! b" passive and b" active components in t!e musculoskeletal
s"stem( Re%ular dense connective tissue structures suc! as li%aments conve" 3transmit5 t!ose
$orces .passivel"(.
From !ere on, t!e term .connective tissue,. i$ not indicated ot!erwise, is used in t!e narrow
meanin% o$ .re%ular dense 3colla%enous5 connective tissue. 3RD0)5( Suc! structures can transmit
onl" in a ver" particular position o$ t!e oint,t!at is, w!en t!e" are stretc!ed and loaded( )!at is
w!" t!is met!od o$ $orce transmission is called .passive(. 1uscles can transmit $orce in var"in%
oint positions because t!e" can activel" c!an%e and adapt t!eir len%t!( *natomicall", t!e two
main components o$ t!is s"stem, t!at is, muscles and li%aments,are %enerall" t!ou%!t to be
or%ani+ed in parallel, 1uscles can control oint stabilit" in t!e w!ole ran%e o$ motion, li%aments
onl" in a particular oint position( )!is means t!at t!e periarticular connective tissue, suc! as
capsules and li%aments, w!ic! also pla" roles in providin% mec!anoreceptive in$ormation to t!e
central nervous s"stem, can be tri%%ered onl" in a particular oint position,t!at is, w!en t!e
relevant connective tissue is stretc!ed or loaded(
*natomists o$ t!e ?niversit" 1aastric!t, Eet!erlands,
3D9445
started to stud" t!e arc!itecture o$
RD0) comple2es in t!e musculoskeletal s"stem bot! %loball" and speci$icall" in t!e cubital re%ion(
)!e" $ound t!at, in t!e !uman elbow oint, passive conve"ance o$ tensile stresses does not occur
t!rou%! capsular li%aments alone( &n a simulation model o$ t!e !uman elbow oint, t!e reaction
$orces resultin% $rom t!e $orces o$ t!e biceps and brac!ioradialis muscle activit" and an applied
e2ternal load s!owed onl" a small di$$erence between simulations wit! an intact capsule 3includin%
li%aments5 and simulations wit! t!e capsule sectioned(
3475
)!ese and ot!er $indin%s c!allen%ed
notions about t!e mec!anical arc!itecture o$ t!e periarticular structures in t!at re%ion and t!eir
role in transmittin% $orces and stresses alon% t!e elbow oint( Our team at t!e ?niversit"
1aastric!t t!ere$ore developed a new tec!ni-ue o$ dissection to e2plore t!ese anatomic
relations!ips(
)!e central prere-uisite in t!e .alternative. dissection procedure t!at !as been developed was to
maintain continuit" o$ t!e connective tissue b" a connective tissue sparin# dissection
procedure( &n t!e dorsolateral antebrac!ial and elbow re%ion, t!e antebrac!ial $ascia 3$ascia
antebrac!ii5 was not removed, but was opened b" lon%itudinal incisions parallel to t!e lon% a2is o$
t!e super$icial e2tensor muscles underneat!( )!e $ascia was t!en released $rom t!e muscle $ibers
o$ t!e underl"in% muscles( &n t!e distal t!ird o$ t!e so#called muscle bellies, w!ere t!e muscle
$ibers convert to t!e perip!eral tendons o$ t!e muscles, t!is separation $rom underl"in% muscle
tissue was easil" made 3Fi%( 45( Fere, underneat! t!e $ascia, a .%lidin% and slidin%. la"er o$ loose
areolar tissue was $ound, similar to tissue in areas o$ tendinous bursae( Fere, t!e muscles o$ t!e
dorsal antebrac!ial re%ion appear as t!e anatomicall" separated structures and entities t!at t!e"
are conceptuali+ed to be in anatom" dissections and te2tbooks( )!e connective tissue and $ascia
involved serves as a %lidin% and slidin%,t!at is, .disconnectin%.,medium(

FIG. 1, 'pening of the antebrachial fascia in the distal forearm re-gion, 0ntermuscular loose areolar connective
tissue revealed be-t*een the discrete muscle bellies and tendons, Left arm, dorsal side, lateral vie*,

Fowever, in t!e pro2imal !al$ o$ t!e $orearm, t!e situation is ver" di$$erent 3Fi%( 75( Fere, t!e
muscle $ascicles ori%inate $rom t!e antebrac!ial $ascia in an obli-ue or pennate con$i%uration( Onl"
a s!arp cuttin% procedure could .remove. t!e $ascia $rom t!e underl"in% muscle $ibers( )!ose
pro2imal muscle bell" $ibers were also ti%!tl" connected wit! stron% intermuscular connective
tissue la"ers immediatel" continuous wit! $ascia antebrac!ii( So, in t!e pro2imal lateral cubital, t!e
arc!itecture o$ t!e $ascial connective tissue is -uite di$$erent $rom t!at in t!e distal re%ion: a
comple2 apparatus o$ RD0) la"ers is situated on top, between, and deep to t!e muscles( )!e
la"ers t!emselves are continuous wit! eac! ot!er, $ormin% walls o$ muscle compartments 3cases5(
)!e muscle $ibers ori%inate in an obli-ue or pennate con$i%uration $rom t!ose compartment walls;
t!e walls, in t!eir turn, conver%e toward t!e lateral !umeral epicond"le( &n $act, anepicondylar
connective tissue apparatus serves as t!e insertion area $or t!e nei%!borin% muscle $ibers( )ensile
$orces are t!ere$ore transmitted $rom t!e muscle $ibers to t!e lateral !umeral epicond"le via t!ese
conver%in% la"ers o$ RD0)( Eo muscle $iber inserts directl" to t!e epicond"le( Onl" t!e most
super$icial part o$ t!e e2tensor carpi radialis muscle ori%inates $rom t!e supracond"lar !umeral
periosteum( &n addition, in t!e pro2imal lateral cubital re%ion, colla%enous $ibers do not run $rom
bone to bone as is usuall" t!ou%!t( 1ost o$ t!e colla%enous $ibers in t!e pro2imal lateral cubital
re%ion appear to be interposed between skeletal tissue and muscle $ascicles( )!ere$ore no
separate entit" suc! as a collateral radial ligament could be demonstrated(
F(2' 3( )!e compartment walls o$ t!e pro2imal muscle compartment o$ t!e t!ird e2tensor di%itorum muscle are
opened and separated $rom t!e muscle $ibers( <e$t arm, dorsal side, lateral view(

Not In Pa!allel 0$t In Se!ies
&n a .re%ular. dissection procedure, t!e ne2t step is t!at t!e muscles are dissected and taken
out( )!e scalpel !as to cut s!arpl" awa" t!e pro2imal muscle bellies o$ t!e e2tensor muscles, in
t!is wa" leavin# in situ stron% bands o$ colla%enous connective tissue t!at could be identi$ied as
collateral radial li%ament( &n t!e connective#tissue sparin% dissection, t!e muscle $ibers are
removed and t!e alread"#mentioned epicond"lar connective tissue apparatus is revealed( )!e
RD0) strands t!at are usuall" identi$ied as collateral li%ament are indeed an inte%ral part o$ t!e
epicond"lar connective tissue apparatus, meanin% t!at, in re%ular dissection, t!e collateral radial
li%ament is dissected out as an arti$actG )!is is demonstrated in Fi%s( : and 6(

F(2' 4( Hro2imal lateral elbow re%ion( 1uscles are dissected awa" $rom t!e epicond"lar connective tissue
apparatus and re$lected 3to t!e le$t5( )!e conver%ence o$ t!e remainin% connective tissue muscle compartment
walls toward t!e lateral !umeral epicond"le is clearl" demonstrated( <e$t elbow, lateral view(

F(2' 5( Hro2imal lateral $orearm re%ion( 1uscles and muscular tis#sue !ave been removed( )!e most pro2imal
e2tensions o$ t!e muscle compartment walls 3t!e epicond"lar connective tissue apparatus5 are le$t in situ,
demonstratin% t!e muscle compartments conver%in% to t!e lateral epicond"le( <e$t elbow, lateral view(

)!e same situation appears to be true $or t!e annular radial li%ament( )!e pro2imal portion o$ t!e
supinator muscle appears as a broad and lon% aponeurotic structure( )!is aponeurosis mer%es
wit! t!e ot!er la"ers and is an inte%ral part o$ t!e epicond"lar connective tissue apparatus
conver%in% to t!e lateral !umeral epicond"le( 6ot any muscle $iber o$ t!e supinator muscle !as a
bon" insertion on t!e !umeral epicond"le itsel$(
*%ain, w!en t!e supinator muscle is dissected as an .entit",. a strand o$ colla%enous connective
tissue remains t!at mi%!t be identi$ied as annular li%ament( Fowever, t!e colla%enous $ibers o$ t!is
band run in pro2imodistal direction and not in a circumradial direction as is usuall" represented in
anatom" books( &$ an annular radial li%ament is dissected, it will e2!ibit cut ed%es, indicatin% t!at,
a%ain, a mec!anical continuit" !as been distorted in t!e e$$ort to dissect li%aments and muscles as
parallel structures( &n $act t!e so#called annular li%ament does not e2ist; it is an inte%rated part o$
t!e aponeurotic la"er o$ connective tissue via w!ic! supinator muscle $ibers insert to t!e lateral
epicond"le( )!is la"er in turn is an inte%rated part o$ an epicond"lar connective tissue apparatus(
)!e pro2imal lateral cubital re%ion !olds a comple2 apparatus o$ RD0) la"ers t!at mainl" consist
o$ muscle compartment walls t!at conver%e toward t!e lateral !umeral epicond"le( Onl" a sin%le
muscle, t!e anconeus, inserts directl" into t!e !umeral periosteum as seen earlier wit! t!e
e2tensor carpi radialis( Fowever, most colla%enous $ibers in t!e pro2imal lateral cubital re%ion are
interposed between skeletal tissue and muscle $ascicles( Onl" a ver" small portion o$ t!e $ibers run
$rom bone to bone and ma" t!ere$ore be classi$ied as li%amentous $ibers( &ndeed
no separate entities suc! as collateral or annular li%aments can be described( )!is means t!at
most muscle $ibers in t!e pro2imal lateral elbow re%ion are or%ani+ed in series and not in
parallel wit! t!e connective tissue o$ t!is apparatus( )!e muscle7connective tissue units $orm
t!efunctional units t!at transmit tensile stresses over t!e elbow oint, wit! muscular and
colla%enous connective tissue or%ani+ed in series, )!ese units do not coincide wit! t!e usual
anatomic classi$ication into muscles and li%aments( *lt!ou%! suc! $unctional units do indeed
coincide wit! muscles and t!eir distal tendons as bot! $unctional and morp!olo%ic entities in t!e
distal e2tent o$ t!e $orearm, t!e $unctional or%ani+ation is seen to be transmuscular 3or .non#
muscular.5 in t!e pro2imal $orearm re%ion(
)!is arc!itecture !as conse-uences $or conve"in% tensile $orces and stresses over a s"novial oint(
?suall" it is assumed t!at t%o components in t!e musculoskeletal s"stem conve" tensile
mec!anical stresses over s"novial oints: 0) structures suc! as li%aments conve" suc! $orces
passivel", and muscles serve as t!e .active. components, t!e latter structures or%ani+ed in
parallel to t!e $ormer ones( <i%aments can per$orm t!eir $orce#conve"in% $unction onl" in a ver"
particular position o$ t!e articulatin% bones,t!at is, t!e" must be stretc!ed and loaded( On t!e
ot!er !and, muscles are capable o$ t!is $unction in var"in% positions o$ t!e oint, because t!e" are
able to continuousl" adapt in len%t!( Fere, t!is is called t!e in-parallel view, and it is
demonstrated in Fi%( =3a,b5(

FIG. 5, 1a2 !he &classical& in#parallel organi(ation of the iu3taarticular tissue, From inside to outside% articular
capsule 1blue24 reinforcing iu3ta-articular regular dense connective tissue structures 1ligaments2 1yello*24 and
on the outer side, periarticular muscle 1red2, 1b2 !he &classical& organi(ation principle of iu3ta-articular
connective tissue running from bone to bone, organi(ed in parallel to the muscular component 1tendons2, 'nly
in a particular 5oint position can the connective tissue transmit forces or signal in the sense of mechanoreceptor
triggering 16666 versus 77772,

&n an in-series con$i%uration as alternativel" described !ere, t!e conve"in% o$ tensile stresses b"
t!e colla%enous $ibers also depends on t!e muscle $ascicles t!at are active( &n vivo displacement o$
bones and muscular activit" in$luence t!e state o$ stress and tension o$ connective tissue
elements( &n t!is model, passive and active oint#stabili+in% structures or%ani+ed in parallel,t!at
is, muscles and li%aments wit! mutuall" independent $unctions,cannot be distin%uis!ed( )!e oint
capsule and its rein$orcements no lon%er !ave an e2clusive role in t!e passive conve"in% o$ tensile
stresses( )!e $unctional units involved in t!e transmission o$ $orces do not consist o$
topo%rap!icall" de$ined and separate entities o$ either muscular orli%amentous tissue(
For instance, a structure suc! as t!e supinator aponeurosis ma" be classi$ied as epim"sial $ascia,
but also as an aponeurosis or even as a .li%ament. wit! adustable len%t! and tension: a
.d"nament. 3discussed in more detail s!ortl"5( )!e traditional topo%rap!ic approac! to t!e
locomotor apparatus also assumes t!at t!e passive components 3li%aments5 are deep to t!e
super$icial components 3muscles5 t!at are activel" involved in t!e maintenance o$ oint stabilit"
and inte%rit" IFi%( =3a,b5J( )!is concept is c!allen%ed b" t!e in.seriesarc!itecture described !ere(
&n t!e lateral cubital re%ion o$ !umans and rats, no li%aments can be distin%uis!ed as separate
entities( )!ere is one oint stabilit" s"stem, in w!ic! muscular tissue and RD0) interweave and
$unction mainl" in an in series situation as s!own in Fi%( >3a,b5( )!us, in vivo, t!e periarticular
connective tissue is loaded and stretc!ed bot! b" t!e movement o$ related skeletal parts and b"
t!e tension o$ t!e muscle tissue insertin% to t!is connective tissue(
FIG. 6, 1a2 !he alternative in#series organi(ation of the iu3ta-articular tissue, From inside to outside% articular
capsule 1blue24 periarticular regular dense connective tissue 1yello*2 in series *ith periarticular muscle 1red2,
1b2 !he alternative organi(ation of iu3taarticular connective tissue organi(ed in series to the muscular
component, 0n all 5oint positions the connective tissue of the 5oint is brought to tension and is capable of
transmitting forces and signaling in the sense of mechanoreceptor triggering 16666 and 66662,
)!is connective tissue arc!itecture can be better appreciated i$, rat!er t!an talkin% in terms o$
collateral li%aments, a .lateral cubital $orce transmission s"stem. 3<0F)S5 is de$ined
3D5
t!at can be
made visible in a ma%netic resonance ima%in% section o$ t!e re%ion( )!is approac! reveals a
principle t!at can be reco%ni+ed in man" ot!er areas and re%ions o$ t!e bod"( For e2ample, similar
connective tissue arc!itecture !as been described $or t!e opposite re%ion o$ t!e elbow: a .medial
cubital $orce transmission s"stem(. )!e in-seriescontinuit" o$ t!e patellar retinacula 3includin%
parts o$ t!e so#called collateral li%aments o$ t!e knee oint5 wit! t!e vastus medialis and vastus
lateralis muscles demonstrates t!e same principle( Similar arc!itectural relations!ips are seen $or
t!e $ascia cruris and t!e ventral e2tensor muscles o$ t!e $orele%, or $or t!e erector spinae muscle
and t!e t!oracolumbar $ascia(
A!c#itect$!al Units of
Connecti'e and M$sc$la! Tiss$e
Detailed studies o$ t!e lateral cubital re%ion o$ t!e rat 3discussed later in t!is article5 s!owed t!is
arc!itecture(
34C5
1ost deep and super$icial RD0) la"ers 3as muscle compartment walls5 are
or%ani+ed in series wit! muscle $ascicles( 0olla%enous $ibers runnin% $rom bone to bone,t!ou%!t
to be stressed passivel" b" displacement o$ t!e articulatin% bones,!ardl" occur( &nstead, t!ere
occur broad aponeurotic la"ers o$ RD0) to w!ic! relativel" s!ort muscle $ascicles insert, w!ic!, on
t!e opposite side, are directl" attac!ed to skeletal elements( Suc! con$i%urations o$ muscle
$ascicles attac!ed to t!e periosteum o$ one articulatin% bone and via a la"er o$ RD0) indirectl"
attac!ed to anot!er articulatin% bone, could be considered .d"namic li%aments(. Suc!
.d"naments. are not necessaril" situated directl" beside t!e oint cavit" or in t!e deep part o$ t!e
oint re%ion(
/" describin% t!e d"nament as an arc!itectural unit o$ t!e musculoskeletal s"stem, we mean a
unit o$ RD0) connected to t!e periosteum o$ a skeletal element wit! muscle $ascicles in
series attac!ed to it( &n Fi%( A3a5 a d"nament is represented in its most basic appearance: a
unipennate muscle between two skeletal elements( * t"pical unipennate $orearm muscle as
represented in Fi%( A3b5 s!ows t!e common appearance o$ t!e d"nament( &n t!is situation, t!e
distal RD0) element is represented b" t!e tendon and is situated intramuscularl"( )!e pro2imal
RD0) element is represented b" one o$ t!e muscle compartment walls and is
situated e&tramuscularl"(

FIG. 7, 1a2 Schematic diagram of the &dynament& as architectural unit, A regular dense 1collagenous2
connective tissue 1+D8!2 layer 1top, yello*2 *ith inserted muscle portion 1middle, red2, Morphologic substrate
of proprioception indicated *ith blue dots 1L8, +87.!', see te3t2 and red stripes 1muscle spindles2, Afferent
nerve indicated 1on top, blac92, ote that the innervation pattern of the muscle-related mechanoreceptors
resembles the innervation pattern of a 5oint capsule 1from outside to inside2, 1b2 An unipennate forearm muscle
as typical &dynament,& )ro3imal 1top left, light grey2, an +D8! layer 1membrane, aponeurosis, septum, etc,2
*ith muscle fascicles attached to it, mostly e3tramuscular 1middle, striated red2, Distal 1bottom right, dar9
grey2, an +D8! layer 1tendon, aponeurosis, etc,2 *ith muscle fascicles 1middle, striated2 attached to it, mostly
intramuscular, 0n this basic situation, the muscle component is organi(ed as intermediate bet*een t*o +8D!
structures,

Distal $orearm e2tensor carpi radialis brevis muscles and e2tensor di%itorum muscles clearl" s!ow
t!is t"pe o$ $unctional unit IFi%( B3c5J( )!e supinator muscle s!ows a variant con$i%uration, wit!
distal connective tissue la"ers t!at are well developed, but wit!out an e2tensive connective tissue
apparatus intermediatin% at t!e insertion IFi%( B3b5J( )!e lon% !ead o$ t!e triceps s!ows a similar
orientation but in t!e .opposite direction. IFi%( B3d5J, wit! developed connective tissue la"ers
pro2imall" rat!er t!an distall"( &$ neit!er a .pro2imal. nor a .distal. connective tissue apparatus
!as been developed, t!e result is a muscle .wit!out aponeurosis or tendon.,$or e2ample, t!e
deltoideus muscle IFi%( B3a5J( &$ t!e muscular connectin% and intermediatin% tissue !as completel"
.disappeared,. a li%ament is t!e conse-uence IFi%( B3e5J(

FIG. 8. 1a,b,c,d,e2 )ossible appearances of the &dynament& as architectural unit, 0n the middle 1c2, the basic
situation :see Fig, ;1b2<, 'n the left 1b2, muscle tissue pro3imally inserting directly to the s9eletal element
1periosteum2 and distally via tendons, 'n the right 1d2, muscle tissue distally inserting directly to the s9eletal
element 1periosteum2, pro3imally via septa and aponeuroses, 'n the e3treme left 1a2, only muscular fascicles,
no intermediating regular dense connective tissue 1+D8!2 structure=a &typical muscle,& 'n the e3treme right
1e2, no muscle tissue intermediating, only +D8!=a &typical ligament,&

&n $act, li%aments, de$ined as strands o$ RD0) runnin% $rom t!e one skeletal element to t!e ne2t,
are an e2ception( )!e" have to $e an e2ception( )!e RD0) !as tissue properties o$ !i%!
resistance to loadin%, a !i%! de%ree o$ !"steresis, and little elasticit"; a li%ament as interposed
structure between two mova$lebones can t!ere$ore be constructed onl" i$ t!e distance between
t!e opposite points o$ li%amentous insertion on t!e bones c!an%es ver" little durin% t!e ran%e o$
motion o$ t!e oint( )!is re-uires speciali+ed desi%n in t!e con$i%uration o$ t!e bones and t!e oint
3sur$aces5, and t!ere are onl" a $ew e2amples o$ suc! .true. li%aments at oints in t!e bod":
cruciate li%aments o$ t!e knee oint or li%amentum apicis dentis in t!e atlantooccipital oint(
O$ course in t!e .classical. $ibrous oints, t!e li%amentous or%ani+ation principle is clearl" present,
but in suc! cases, t!is or%ani+ation is consistent wit! t!e wa" suc! oints are $unctionall" loaded(
Suc! con$i%urations could t!ere$ore be considered e2tremes to t!e %eneral rule( &t bears repeatin%
t!at t!ese p!enomenolo%ic and $unctional considerations do not tell an"t!in% about t!e conditions
in and b" w!ic! t!ose tissues and structures di$$erentiate(
*n arc!itectural approac! to t!e anatom" o$ t!e locomotion s"stem as practiced !ere s!ows t!at
$asciae e2!ibit a variet" o$ mec!anical relations!ips wit! nei%!borin% tissue and t!ere$ore ma"
pla" -uite di$$erent $unctional roles( Sometimes t!e" act as aponeuroses, sometimes t!e" are
%lidin% envelopes buildin% oint#like %lidin% spaces( )!e nomenclature .$ascia. s!ould t!ere$ore be
considered and reevaluated criticall" in ever" re%ion( )!e .classical. $asciae o$ t!e or%ans and o$
muscles usuall" represent t!e .%lidin% $asciae. t"pe 3a%ain, we consider t!e coelom as a kind o$
.oint space.5( 1an" epim"sial muscle $asciae $unction in a similar wa"( Fowever, a $ascia suc! as
t!e $ascia cruris or t!e retinaculum patellae $unctions as an epimuscular aponeurosis(
)o understand t!e mec!anical and $unctional circumstances $or t!e $ascial role in connectin% and
conve"in% stresses, it is more important to know t!e architecture o$ t!e connective and muscle
tissue t!an t!e re%ular anatomical order or topo%rap!"( &n principle, t!is approac! applies to ever"
$ascial la"er in t!e !uman bod"( One must know $oth w!ere t!e" are situated 3.anatom".5
and ho% t!e" are connectin% and connected 3.arc!itecture.5(

THE ARCHITECTURE OF CONNECTI+E TISSUE AS INSTRUMENTAL FOR
PROPRIOCEPTION IN THE LOCOMOTOR APPARATUS
T#e S$0st!ate of P!o*!ioce*tion
)!e arc!itectural view developed !ere !as implications $or t!e understandin% and interpretation o$
t!e spatial or%ani+ation o$ t!e nervous a$$erents, wit! related receptors t!at $orm t!e substrate $or
proprioception( W!at kind o$ role does t!e arc!itecture in t!e musculoskeletal s"stem pla" in t!e
-ualit" o$ centripetal in$ormation $rom t!e various components and tissues o$ t!e s"stem8
)!e usual distinction between muscle a$$erents and articular a$$erents is implicitl" based on t!e
anatomical concept t!at 3peri5articular RD0) structures and muscular tissue structures are
or%ani+ed in parallel to eac! ot!er alon% t!e oint( )!is latter concept is t!e one t!at was
c!allen%ed in t!e previous part o$ t!is essa"(
0onnective tissue and $asciae are ric!l" innervated(
3:,75
Fascial la"ers ma" t!us pla" an important
role in proprioception and nociception( 0onsiderations suc! as .arc!itecture versus anatom"
3topo%rap!"5,. mutatis mutandis ma" also appl" $or t!e spatial or%ani+ation
o$ mechanoreceptors, t!e morp!olo%ic substrate $or proprioception( )o stud" t!e role and
$unction o$ mec!anoreceptors in t!e process o$ proprioception, it ma" be important to
know %here t!e" actuall" are located in suc! re%ions and !ow t!e" are or are not connected wit!
t!e relatin% tissue elements( )!e actual spatial or%ani+ation o$ suc! receptors can be better
interpreted $unctionall" w!en it is known !ow t!eir topo%rap!" is related to t!e arc!itecture o$ t!e
connective and muscular tissue(
Hroprioception is t!e process o$ conscious and subconscious sensorin% o$ oint position or motion(
Encapsulated or unencapsulated mec!anosensitive sensor" nerve endin%s 3mec!anoreceptors5 and
related a$$erent neurons provide t!e centripetal in$ormation needed $or t!e control o$ locomotion
or $or t!e maintenance o$ posture( &n %eneral, suc! mec!anoreceptors are reported to occur eit!er
as muscle receptors or as oint receptors( 1uscle receptors are mec!anoreceptors present in t!e
muscles, includin% t!eir au2iliar" structures suc! as tendons, aponeuroses, and $asciae( 1uscle
spindles and @ol%i tendon or%ans 3@)Os5 are t!e best#known t"pes o$ suc! receptors(
34:5
Koint
receptors are considered to be situated in oint capsules and related structures, includin%
rein$orcin% li%aments( )!ese receptor t"pes are usuall" ordered accordin% to t!e 3ultra5structure o$
t!e receptor itsel$, p!"siolo%ic $eatures, t"pe o$ a$$erent nerve $iber, and ot!er parameters(
34694A,a5
&n t!e traditional view, oint receptors pla" t!e leadin% role in monitorin% oint position or
movement $or statest!esis and kinest!esis; muscle receptors are rele%ated to motor $unctions t!at
operate at a subconscious or re$le2 level 3reviewed b" 1c0loske"
34B5
and 1att!ews
34D5
5( Fowever,
t!is concept !as been c!allen%ed b" p!"siolo%" investi%ations su%%estin% t!at muscle spindle
a$$erents can also contribute to !uman kinest!esis( 0linical observations in patients w!o retained
t!eir kinest!esis a$ter complete sur%ical removal or interruption o$ oint capsules 3endoprost!eses5
and e2periments t!at tested position#sensin% abilities $ollowin% selective anest!esia o$ oint
capsules in vivo provided $urt!er evidence t!at muscle spindles 3and mec!anoreceptors o$ t!e
skin5 also contribute to kinest!esis(
37C97:5
&t is o$ten stated t!at oint receptors react onl" at t!e
e2tremes o$ oint position, actin% as .limit detectors.(
3765
&ndeed, it !as been $ound t!at t!e
disc!ar%e o$ articular receptors is limited to positions t!at si%ni$icantl" stress t!e oint capsule,
positions in w!ic! t!e capsule and related structures are supposed to be strained passivel"(
34B,7=9
7B5
Ot!er studies su%%est t!at muscle a$$erents provide t!e substrate o$ mid#or $ull#ran%e receptor
activit" 3or bot!5 present in recordin%s $rom articular nerves(
34B,7>9:45
&n t!eir well#known studies,
*bra!ams, Ric!mond, and /akker describe in t!e neck re%ion o$ t!e cat a variet" o$ sensor"
endin%s in so#called non#articular connective tissue( &n neck proprioception, t!e" su%%est
attributin% a more important role o$ mec!anoreception to substrate t!at is not situated directl"
wit!in or near oint capsules(
3:79:65
1ec!anoreceptors are in $act $ree nerve endin%s 3FEEs5, w!et!er or not e-uipped wit! speciali+ed
end or%ans( )!e main stimulus $or suc! receptors is de$ormation( Lariation e2ists as to t!e
microarc!itecture o$ t!e endin%( On t!e one !and, t!ere e2ists t!e principle o$ lamellae around a
relativel" simple nerve endin%( )!is represents t!e principle o$ t!e ball# or bean#s!aped Later
Haccini or pacini$orm corpuscles, o$ten called lamellated corpuscles 3<05( On t!e ot!er !and, t!ere
is t!e more spra"#like or%ani+ation o$ t!e nerve endin% wrappin% around and between t!e
de$ormable substrate#like connective tissue $ibers( )!ose are t!e spindle#s!aped Ru$$ini corpuscles
3R05 or @)Os( )!ese two t"pes o$ microarc!itecture rou%!l" relate to t!e t"pe o$ mec!anical
de$ormation t!at is at stake,t!at is, compression $or t!e lamellated bodies and traction and
torsion $or t!e spra"#like t"pe( Ot!er var"in% parameters are t!res!old, adaptivit", and
adustabilit"( &n t!is %eneral classi$ication, t!e muscle spindle is a spindle#s!aped spra"#like endin%
or%ani+ed around speciali+ed muscle $ibers e-uipped wit! t!e e2tra possibilit" o$ adustable len%t!(
1ec!anoreceptors associated %ith muscles, includin% t!e muscle au2iliar" structures suc! as
tendons, are usuall" classi$ied
34694A5
as $ollows:
FEEs 3unencapsulated5
1uscle spindles 3sensor" endin%s wit! encapsulated intra$usal muscle $ibers5
@)Os 3t"pe &&& endin%s, relativel" lar%e,4CC 9 >CC Mm diameter,spra"#like
endin%s, wit! !i%! t!res!old and ver" slow#adaptin%5
)!e mec!anoreceptors t"picall" associated wit! oints are t!ese:
FEEs 3unencapsulated5
<0s 3t"pe && endin% wit! a two# to $ive#la"ered capsule, less t!an 4CC Mm in len%t!, wit!
low t!res!old and rapidl" adaptin%5( Fere, t!is term is pre$erred to pacini$orm corpuscle(
R0s 3t"pe & endin%, relativel" small,up to 4CC Mm,spra"#like endin% wit! low t!res!old
and slow#adaptin%5
S*atial Dist!i0$tion of Mec#ano!ece*to!s as F$nctional Pa!amete!
)!e assumption o$ an in-series or%ani+ation o$ muscular and colla%enous connective tissue instead
o$ an in-parallel or%ani+ation stron%l" in$luences t!e view o$ t!e areas t!at ma" be considered to
be most .strate%ic. $or mec!anoreception based on de$ormation or ot!er mec!anical stimuli(
De$ormation is e2pected to be !i%!est in t!e transition between tissues o$ t!e musculoskeletal
s"stem wit! di$$erent consistencies and mec!anical -ualities( Similar considerations !old $or t!e
transitional areas o$ muscular and colla%enous connective tissue wit! skeletal tissue(
)went"#$ive "ears a%o, our researc! %roup at 1aastric!t ?niversit" proposed t!is -uestion: &s
t!ere a correlation between t!e arc!itecture o$ t!e muscular and connective tissue and t!e spatial
distribution 3.arc!itecture.5 o$ t!e morp!olo%ic substrate o$ proprioception8
&n t!e rat, innervation o$ t!e RD0) apparatus in t!e pro2imal lateral elbow re%ion was studied
usin% various tec!ni-ues and reconstructed t!ree#dimensionall" in relation to t!e arc!itecture o$
muscle and connective tissue(
34C,445
)!e $indin%s $rom t!ose studies s!owed t!at no
mec!anosensitive nerve terminals are present%ithin t!e stress#conve"in% components o$ t!e
epicond"lar connective tissue apparatus( Fowever, FEEs are $ound in t!e transitional areas o$ t!e
connective tissue apparatus towards t!e periosteum( Harticularl" in t!e outer 3epim"sial5 and in
some intermuscular components o$ t!e apparatus, ple2i$orm#arran%ed nerve $ascicles can be
demonstrated( /esides autonomic nerve $ibers, t!e" contain %roup &&& 3*#delta5 and %roup &L 3095
nerve $ibers( )!ose nerve $ibers are involved in t!e a$$erent pat!wa" o$ proprioceptive in$ormation
$rom t!e transitional areas between t!e connective tissue la"ers and t!e muscle $ascicles
or%ani+ed in series wit! t!em Is!own sc!ematicall" in Fi%( A3a5J( )!is also seems to represent a
more li%amentous or articular .pattern o$ innervation. compared wit! t!e related nerve $ascicles
runnin% on t!e .outside. o$ t!e innervated structure( )!is is actuall" a t"pical capsular or articular
pattern Isee Fi%( A3a5J( Suc! ple2uses are also ver" dominantl" present on t!e so#called ante#
brac!ial $ascia( )!e nerve $ascicles o$ suc! substrate terminate in <0s, R0s, @)Os, FEEs, and
3sometimes5 muscle spindles(
* spectrum o$ mec!anosensitive substrate occurs at t!e transitional areas between t!e RD0)
la"ers and t!e muscle $ascicles or%ani+ed in series wit! t!em( )!is substrate e2!ibits $eatures o$
t!e mec!anosensitive nerve terminals t!at usuall" are considered to be c!aracteristic $or .oint
receptors. and $or .muscle receptors(. For e2ample, t!e olecranal retinaculum and t!e supinator
aponeurosis 3and its pro2imal continuation wit! t!e epicond"lar connective tissue apparatus5 wit!
t!e muscle $ascicles in series to t!ose la"ers are well#e-uipped wit! suc! morp!olo%ic substrate(
)!e !uman e-uivalents o$ t!ese structures are, respectivel", t!e aponeurosis o$ t!e supinator
muscle and t!e tendon o$ t!e triceps muscle(
/ased on arc!itecture and spatial distribution o$ t!e substrate o$ mec!anoreception, it ma" be
assumed t!at t!e .oint receptors. !ere are also in$luenced b" t!e activit" o$ t!e muscle or%ani+ed
in series wit! t!e colla%enous connective tissue near t!ose receptors( )!e pro2imal e2tensions o$
t!e muscle compartment walls are well#e-uipped wit! mec!anosensitive substrate( )!is supports
t!e idea t!at t!e stresses durin% oint positionin% are conve"ed mainl" via t!ose colla%enous
la"ers and also are involved in tri%%erin% t!e related mec!anoreceptors( &n t!e studied re%ion,
t!ere e2ists no basis in morp!olo%" $or so#called oint receptors t!at are de$ormed e2clusivel" b"
passive strain in colla%enous connective tissue structures induced b" displacement o$ t!e
articulatin% bones(
)!e demonstrated substrate o$ proprioception also caused trouble as to morp!olo%ic classi$ication(
)!e t"polo%" and spectrum o$ nerve $ascicles and nerve terminals $ound !ere e2!ibit $eatures
usuall" associated wit! tendons as well as wit! oint capsules and li%aments(
Summari+in%, t!en, we !ave encountered
an .e2ternal. pat!wa" $or t!e a$$erent nerve $ibers Isee also Fi%( A3a5J(
t!e presence o$ %roups &&& and &L nerve $ibers(
t!e presence o$ nociceptive, but also putativel" mec!anoreceptive FEEs(
t!e occurrence o$ .Ru$$ini#like. or .@)O#like. corpuscles at t!e transitional +one between
colla%enous connective tissue la"ers and insertin% muscle $ascicles 3receptors t!at e2!ibit $eatures
t!at could lead to classi$ication as @)Os5(
t!e occurrence o$ <0s in transition +ones between RD0) la"ers and ot!er nearb" reticular
colla%enous connective tissue or insertin% muscle $ascicles(
)!e substrate o$ proprioception t!at we $ound in and near t!e RD0) apparatus !as $eatures o$
mec!anoreceptors t!at usuall" are linked wit! .oint receptor. substrate and wit! t!e
mec!anoreceptors usuall" present in muscles and related tendons(
)!e $indin%s re%ardin% spatial distribution and or%ani+ation o$ t!e mec!anoreceptive substrate t!at
is usuall" accepted as muscle receptors,t!at is, t!e muscle spindles and @)Os,were even
more suitable wit! t!e concept t!at is brou%!t $orward !ere( )!e latter receptors are not
or%ani+ed accordin% to principles o$ anatom" and topo%rap!", but accordin% to t!e $unctional
arc!itecture o$ RD0) la"ers in relation to muscular arc!itecture( &n Fi%( D3a,b5, it is clearl" s!own
t!at, in all t!e studied antebrac!ial e2tensor muscles, t!e distribution o$ muscle spindles per
muscle area is uneven( &$ t!e spatial distribution o$ muscle spindles is considered per muscle, it is
di$$icult to detect a common distribution pattern in all muscles( /ut considerin% muscle spindle and
@)O distribution .transmuscularl". reveals ot!er $unctional aspects o$ t!e distribution pattern( )!e
spatial distribution and orientation o$ t!e spindles 3includin% t!e distribution o$ @)Os5 is
understandable onl" $rom t!e re%ional $unctional arc!itecture o$ t!e RD0) structures( )!e
muscular +ones t!at are dense in muscle spindles and @)Os are t!e stress# and $orce#conve"in%
+ones o$ t!e muscle t!at are in series wit! t!e <0F)S distally and in series wit! t!e perip!eral
tendons pro&imally( )!is arran%ement provides a common principle t!at ma" e2plain man" kinds
o$ distribution patterns( *nd, o$ course, sometimes arc!itectural units coincide wit! speci$ic
topo%rap!ic entities(

FIG. 9 1a2 !he spatial distribution of muscle spindles in the superficial lateral forearm muscle in the rat, !he
distribution is clearly more related to the architecture of the pro3imal epicondylar connective tissue apparatus
than to the topography of the muscles, !he spindles are presented as thin blac9 lines, !he thic9er lines in the
diagram represent the intermuscular septa that are part of the pro3imal regular dense connective tissue
1+D8!2 apparatus 1blue, on the left2 and the distal tendons of the superficial e3tensor muscles 1red, on the
right2, 1b2 !ypical cross-sections of a rat forearm 1four pro3imal sections from a total of si3 forearm sections2,
!he muscle spindles and .olgi tendon organs 1.!'s2 in a given segment are pro5ected onto each section in a
summative pro5ection, Dots are muscle spindles, stars are .!'s, ote that .!'s are not only present near or
at distal tendons, the pro3imal intermuscular septa and fasciae also have .!'s arranged to it,

P!o*!ioce*tion(Not Only a Matte! of Anatomy 0$t Also of A!c#itect$!e
We !ave demonstrated t!at muscle spindles and @)Os occur in muscular tissue areas in
series wit! RD0) structures( Suc! an area does not o$ten coincide wit! a morp!olo%ic muscle
entit"( )!e arc!itectural relation between t!e RD0) structures seems to de$ine t!e spatial
distribution o$ spindles and @)Os in t!e re%ion as a w!ole( We identi$ied 3sub5units o$ muscular
tissue in series wit! RD0), so#called muscle spindleN@)O +ones, wit! a relativel" !i%! densit" o$
mec!anoreceptors( )!e patterns o$ distribution and orientation in suc! +ones are understandable
$rom t!e perspective o$ t!e arc!itecture o$ t!e muscular tissue related to t!e connective tissue
arc!itecture(
1uscle spindles and @)Os are concentrated mostl" in areas o$ muscular tissue directl"
intermediatin% distal and pro2imal RD0) structures,t!at is, tendons distall", compartment walls
pro2imall"( &$ distal and pro2imal RD0) structures are situated at a relativel" lar%e distance $rom
eac! ot!er, t!e receptors accordin%l" $orm small elon%ated +ones se%re%ated $rom surroundin%
e2tra$usal $ibers 3see Fi%( 4C, patterns 4 and 75( &$ t!e distance between distal and pro2imal RD0)
structures is relativel" s!ort, bot! structures are situated more in parallel wit! eac! ot!er: t!e
spindles run obli-uel" in parallel to eac! ot!er in a relativel" broad muscular area brid%in% a s!ort
distance( (ndividual @)Os occur in a direct one#to#one relation to individual spindles in a
relativel" broad area o$ muscleNconnective tissue transition( )!e e2tra$usal $ibers are more or less
e-uall" distributed between t!em 3see Fi%( 4C, patterns : and 65( 1uscle portions t!at do not link
two RD0) structures, but t!at attac! directl" to periosteal tissue, tend to be devoid o$ muscle
spindles(

FIG. 10, !ypical patterns for muscle spindle>.olgi tendon organ moni-tor (ones 1see te3t2, !he configuration
as sho*n at ? 1right2 repre-sents the typical pattern of a @dynament,A :See also Fig, ;1a2<,

*n in series unit o$ muscular tissueNRD0) la"erN skeletal element e-uipped wit! mec!anosensitive
substrate at t!e transitional areas between t!e various tissue components constitutes t!e basic
unit o$ t!e spatial or%ani+ation o$ t!e substrate o$ proprioception( Suc! a unit ma" occur as a
muscle $raction in series wit! a muscle compartment wall t!at is s!ared wit! t!e muscular tissue
o$ an adacent muscle( &t ma" also appear as a muscle compartment wall wit! muscle $ascicles
insertin% unilaterall" and wit! a$$erent nerve $ibers reac!in% t!e related mec!anoreceptors $rom
t!e outer side( )!is was introduced earlier as t!e t"pical .d"namic li%ament. 3d"nament,see Fi%(
4C, pattern 65(
&$ t!e number o$ mec!anoreceptors is calculated 3per wei%!t or per volume5, t!e outcome
depends not onl" on t!e number o$ receptors, but also on t!e e2tension, volume, or ma%nitude o$
t!e unit t!at is taken into account( )!is $indin% is a%ain determined b" !ow t!e entities in t!e
locomotor apparatus are conceived o$( &n t!e model proposed !ere, neit!er individual muscles nor
li%aments are t!e $unctional entities to w!ic! receptor distribution in t!e relevant oint re%ion
s!ould be related(
For e2ample, muscles wit! similar -uantitative densities appeared to e2!ibit completel" di$$erent
distribution patterns, and t!ose wit! similar distribution patterns s!owed di$$erent densities(
Similar considerations are valid bot! $or absolute and $or relative receptor volumes, because
-uanti$"in% receptors per muscle or per connective tissue structure i%nores t!e $unctional
arc!itectural continuit" in t!e various tissue elements o$ t!e locomotor apparatus t!at maintains
oint inte%rit"( Ouantitative parameters o$ mec!anoreceptors $ail to e2press t!e $unctionalit" o$
t!eir spatial distribution related to t!e arc!itecture o$ muscle and connective tissue( For e2ample,
muscle spindle densit" ma" make more sense reported b" a 3oint5 re%ion or a 3peri5articular area
t!an b" muscle(
*not!er direct conse-uence o$ t!e concept proposed !ere is t!at t!e or%ani+ation o$ t!e
morp!olo%ic substrate o$ proprioception s!ould be re%arded in terms o$ $ractions o$ muscular
tissue rat!er t!an in terms o$ muscles( Recent researc! su%%ests t!at, also on t!e level o$ spinal
sensorimotor control, muscles s!ould no lon%er be considered t!e $unctional entit" in t!e
locomotor s"stem(
3:=9:B5
&n addition, t!e or%ani+ation principle o$ neuromuscular muscle
compartments proectin% in a topo%rap!ical or%ani+ation to t!e correspondin% motor nucleus is
t!ou%!t to allow t!e or%anism to di$$erentiate muscle activit" into activit" o$ muscle parts( )!is
concept a%ain matc!es well t!e task#dependent model o$ <oeb: t!at is, t!at motor units are not
necessaril" or%ani+ed wit! respect to individual motor nuclei, but accordin% to be!avioral tasks(
)!e concept o$ t!e locomotor apparatus bein% built up b" arc!itectural units o$ muscular tissue in
series wit! colla%enous connective tissue is more consistent wit! suc! trans# or supramuscular
models t!an is t!e concept in w!ic! muscles $unction as t!e entities t!at maintain oint inte%rit"(
)!e muscle spindles and @)Os in t!e lateral cubital re%ion o$ t!e rat are concentrated in t!ose
areas w!ere 3in view o$ t!e description o$ t!e arc!itecture o$ t!e muscle and tissue5 t!e conve"in%
o$ tensile stresses over t!e elbow oint is e2pected to take place( So t!e spatial or%ani+ation o$
muscle spindles and @)Os in t!e studied re%ion is suc! t!at it enables monitorin% o$ t!e stresses
conve"ed over t!e elbow oint and o$ t!e movements o$ t!e articulatin% bones( )!is or%ani+ation
allows t!ose receptors to be classi$ied in t!is situation also as .oint receptors(. )!e spatial
or%ani+ation s!ows t!e principle t!at mec!anoreceptors are arran%ed in tissue environments t!at
.o$$er. t!em de$ormation( &n t!ese environments, t!e spatial arc!itecture o$ t!e connective tissue
apparatus is a predominant $actor(
&n conse-uence o$ t!e identi$ication o$ an in-series or%ani+ation o$ muscular tissue and RD0)
3mainl" tendons distall" and compartment walls pro2imall"5 attac!ed to skeletal parts 3periosteal
attac!ment5, three confi#uration types o$ mec!anoreceptors can be identi$ied:

1uscle spindles, @)Os, FEEs, and <0s are $ound in areas between muscular tissue and
RD0)( )!is con$i%uration coincides wit! t!e conventional muscle9tendon spectrum o$ sensor"
nerve endin%s(
34:,:D#675

<0s and FEEs are $ound in areas in w!ic! RD0) adoins reticular connective tissue( )!is
con$i%uration coincides mainl" wit! t!e spectrum o$ sensor" nerve endin%s usuall" indicated as
articular receptors(
34=94A,6:96=5

Onl" FEEs are present in t!e transition to t!e skeletal attac!ment 3periosteum5( )!is
con$i%uration coincides wit! t!e endotenonial spectrum o$ sensor" nerve endin%s(
364,67,6>5
&n t!e above#mentioned con$i%urations, R0s are not indicated as a separate cate%or"( )!e @)Os
and R0s are considered to be t!e same receptor type, presentin% %radual di$$erences dependin%
on t!e te2ture o$ t!e surroundin% tissue(
36=,6A,6B5
&t ma" t!ere$ore be stated t!at t!e -uartet 1S9
@)ONR09<09FEE represents t!e complete spectrum o$ mec!anoreceptors in a oint re%ion( &n t!is
wa", t!e t!ree main t"pes o$ so#called muscle receptors,1S, @)O, and <0
34:5
,are combined wit!
t!e t!ree t"pes o$ so#called capsular 3or oint5 receptors,R0, <0, and FEE(
36:5
)!e conclusion is t!at, in vivo, t!e activit" o$ a mec!anoreceptor is de$ined not onl" b" its
$unctional properties, but also b" its arc!itectural environment( &$ *bra!ams, Ric!mond, and
/akker
3:65
state t!at t!e topo%rap!" o$ mec!anoreceptors provides a .subtle comparative $unction
in t!e process o$ sensor" codin% o$ muscle events,. t!e" raise t!e important issue o$ t!e spatial
distribution o$ receptors in t!e process o$ proprioception( )o t!is s!ould be added t!e notion t!at
t!e arc!itecture o$ t!e muscular and connective tissue and conse-uent receptor distribution pla"s
a si%ni$icant role in t!e codin% o$ t!e proprioceptive in$ormation t!at is provided(
AC,NO/LEDGMENT
& wis! to t!ank Hro$essor )!omas W( Findle", 1D, H!D, o$ t!e 0enter $or Fealt!care Knowled%e, L*
1edical 0enter, East Oran%e and Eewark EK, ?S*, $or !is e2tensive e$$ort to read, comment, and
edit t!is article t!orou%!l" and precisel"( * part o$ t!e intelli%ibilit" o$ t!is article is a result o$ !is
tremendous e$$ort to convert m" Dutc! En%lis! to %ood scienti$ic lan%ua%e( )!is e2pression o$
%ratitude also re%ards !is assistant, 1r( )!omas /rown( Fi%ures 4 t!rou%! > are used courtes" o$
t!e Department o$ *natom" and Embr"olo%", ?niversit" o$ 1aastric!t, )!e Eet!erlands(
CONFLICT OF INTEREST
NOTIFICATION
)!e aut!or declares t!at t!ere are no con$licts o$ interest(
COP-RIGHT
Hublis!ed under t!e 0reative0ommons *ttribution Eon0ommercial#EoDerivs :(C <icense (
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8orresponding author% Kaap van der Wal, ?niversit" 1aastric!t, Facult" o$ Fealt!, 1edicine and
<i$e Sciences, Department o$ *natom" and Embr"olo%", HO /o2 >4>, 1aastric!t >7CC 1D
Eet!erlands(
E-mail% walembr"oS!ome(uni#one(nl