Mechanoreceptors in the medial and lateral glenohumeral ligaments of the canine shoulder joint


Grandis, A.; Spadari, A.; Bombardi, C.; Casadio Tozzi, A.; D.S.rdi, N.; Lucchi, M.L.

Veterinary and Comparative Orthopaedics and Traumatology 20(4): 291-295

2007


In order to have a better understanding of the role of ligaments in canine shoulder joint stability, the presence of mechanoreceptors in the medial (MGHL) and lateral (LGHL) glenohumeral ligaments was detected by means of a modified gold chloride stain. Three morphologically distinct mechanoreceptors were identified: Ruffini receptors (type I endings), Pacinian corpuscles (type II endings) and Golgi tendon organ-like receptors (type III endings). These receptors are mainly localized at each end of the ligaments and are prevalently in their glenoid portion. In particular, in the MGHL the highest density was at the cranial arm of the insertion into the scapula. The variety of mechanoreceptors in canine shoulder ligaments might indicate an afferent function in providing the CNS with joint proprioceptive information. Therefore, besides acting as passive mechanical stabilizers, the MGHL and the LGHL may serve as sensory structures, contributing actively to joint stability. Ligamentous injuries which occur in shoulders not only affect mechanical restraint but also alter the proprioceptive input to the CNS by means of disruption of the mechanoreceptors.

Original
Research
©
2007
291
Schattauer
GmbH
Mechanoreceptors
in
the
medial
and
lateral
glenohumeral
ligaments
of
the
canine
shoulder
joint
A.
Grandisl,
A.
Spadari
2
,
C.
Bombardil,
A.
Casadio
Tozzi
2
,
N.
De
Sordil,
M.
L.
Lucchil
'Department
of
Veterinary
Morphophysiology
and
Animal
Productions,
University
of
Bologna,
Ozzano
dell'Emilia,
Bologna,
Italy
2
Veterinary
Clinical
Department
University
of
Bologna,
Ozzano
dell'Emilia,
Bologna,
Italy
Summary
In
order
to
have
a
better
understanding
of
the
role
of
ligaments
in
canine
shoulder
joint
stability,
the
pres-
ence
of
mechanoreceptors
in
the
medial
(MGHL)
and
lateral
(LGHL)
glenohumeral
ligaments
was
detected
by
means
of
a
modified
gold
chloride
stain.
Three
morpho-
logically
distinct
mechanoreceptors
were
identified:
Ruffin'
receptors
(type
I
endings),
Pacinian
corpuscles
(type
II
endings)
and
Golgi
tendon
organ-like
receptors
(type
III
endings).
These
receptors
are
mainly
localized
at
each
end
of
the
ligaments
and
are
prevalently
in
their
glenoid
portion.
In
particular,
in
the
MGHL
the
highest
density
was
at
the
cranial
arm
of
the
insertion
into
the
scapula.
The
variety
of
mechanoreceptors
in
canine
shoulder
ligaments
might
indicate
an
afferent
function
in
providing
the
CNS
with
joint
proprioceptive
information.
Therefore,
besides
acting
as
passive
mech-
anical
stabilizers,
the
MGHL
and
the
LGHL
may
serve
as
sensory
structures,
contributing
actively
to
joint
stabil-
ity.
Ligamentous
injuries
which
occur
in
shoulders
not
only
affect
mechanical
restraint
but
also
alter
the
pro-
prioceptive
input
to
the
CNS
by
means
of
disruption
of
the
mechanoreceptors.
Keywords
Mechanoreceptors,
glenohumeral
ligaments,
shoulder
joint
stability,
dog
Vet
Comp
Orthop
Traumatol
2007
;
20:
291-295
Prepublished
online
July
26,
2007
doi:10.1160/VCOT-07-01-0005
Introduction
Shoulder
joint
stability
is
provided
by
vari-
ous
components:
joint
compression
from
the
cuff
muscles
(1-3),
negative
intra-ar-
ticular
pressure
(3,
4),
the
adhesion-cohe-
sion
mechanism
by
means
of
joint
fluid
(5)
and
by
the
joint
capsule
with
its
associated
glenohumeral
ligaments
(6,
7).
In
the
litera-
ture,
many
authors
have
placed
emphasis
on
the
importance
of
ligaments
in
joint
stabil-
ity.
In
fact,
ligaments
play
a
double
role
in
joint
stability:
they
act
as
a
mechanical
re-
straint
(6,
8,
9)
and,
furthermore,
as
demon-
strated
electrophysiologically,
they
partici-
pate
in
an
important
reflex
between
the
liga-
ments
themselves
and
the
cuff
muscles
(10-12).
The
reflex
originates from
the
mechanoreceptors
present
within
the
liga-
ments.
The
mechanoreceptors
are
mech-
anically
sensitive
neuronal
endings
which
transduce
mechanical
tissue
deformation
that
has
occurred
either
through
voluntary
movement
or
joint
perturbation,
as
frequen-
cy
modulated
signals
to
the
central
nervous
system
through
afferent
proprioceptive
pathways.
Proprioception
can
be
described
as
afferent
information
which
typically
arises
from
peripheral
mechanoreceptors
that
contribute
to
postural
control,
joint
sta-
bility
and
conscious
sensation
of
movement.
Sensation
of
movement
can
be
further
di-
vided
into
joint
position
sense
and
the
detec-
tion
of
passive
movement
sense.
Collec-
tively,
these
two
sensory
modalities
are
commonly
referred
to
as
joint
kinaesthesia.
In
human
medicine,
knowledge
about
the
presence
and
distribution
of
the
mechanore-
ceptors
and
about
the
reflex
has
led
to
im-
portant
findings
regarding
the
basic
con-
cepts
of
treatment
(13,
14),
thus
improving
the
understanding
of
some
pathogenetic
mechanisms
of
shoulder
luxation.
In
fact,
it
has
been
demonstrated
that
shoulder
insta-
bility
is
associated
with
proprioceptive
defi-
cits
(15,
16).
Although
shoulder
joint
stability
is
a
topic
of
great
interest
among
veterinary
or-
thopaedists
(6,
17-22),
until
now
there
have
not
been
any
neurohistological
studies
con-
cerning
the
canine
glenohumeral
ligaments.
Only
a
few
studies
involving
mechanore-
ceptors
in
dog
joints
have
been
carried
out
on
the
knee
joint
(23,
24).
Therefore,
the
present
investigation
was
undertaken
in
order
to
ascertain
whether
canine
medial
(MGHL)
and
lateral
(LGHL)
glenohumeral
ligaments
contain
mechanoreceptors,
and
in
order
to
identify
their
type
and
localization
in
the
hope
of
shedding
light
on
their
spe-
cific
functions.
Materials
and
methods
The
MGHL
and
LGHL
from
both
sides
of
six
fresh
adult
canine
cadavers,
weighing
from
3—
30
kg,
and
of
different
breeds,
were
obtained
at
necropsy.
All
of
the
shoulders
were
free
from
joint
disease.
The
ligaments
were
stained
in
bulk
by
using
the
gold
chloride
method
of
Gairns
as
modified
by
O'Connor
and
Gonzales
(25).
After
staining,
the
tissue
was
dehydrated
and
paraffin-embedded
according
to
stan-
dard
histological
procedures.
The
speci-
mens
were
serially
cut,
50
gm
in
thickness,
along
three
different
planes
(sagittal,
trans-
verse
and
dorsal),
in
order
to
detect
the
three-dimensional
distribution
of
mech-
Received
January
9,
2007
Accepted
February
8,
2007
Vet
Comp
Orthop
Traumatol
4/2007
(a)
( b
)
O
Ruffini
receptors
in
LGHL
(a,
c)
and
MGHL
(b,
d).
(b)
The
receptor
partially
wraps
around
a
blood
vessel
(arrow).
(c)
A
cluster
of
three
type
I
endings.
(a)
and
(b)
bar
=
100µm;
(c)
bar
=
200
j.tm;
(d)
bar
=
50
gm.
Gold
chloride.
292
Grandis
et
al.
anoreceptors
in
the
ligaments.
The
sections
were
mounted
on
slides,
coverslipped
and
observed
with
a
light
microscope
(Zeiss,
Axioplan).
According
to
the
Morisawa
pro-
cedure,
the
following
three
conditions
were
required
for
the
identification
of
the
nerve
endings:
i)
the
specific
morphology;
ii)
con-
firmation
of
the
morphology
in
serial
sec-
tions;
iii)
the
presence
of
nerve
fibres
in
the
vicinity
(26).
The
nerve
endings
were
classi-
fied
based
on
studies
by
Freeman
and
Wyke,
(27)
and
Morisawa
(26).
The
images
were
recorded
on
a
Polaroid
DMC
digital
photo
camera
(Polaroid
Cor-
poration,
Cambridge
MA,
USA)
and
DMC2
software
and
further
processed
by
using
Adobe
Photoshop
Element
software.
KS
300
Zeiss
software
(Kontron
Elektronik,
Eching,
Germany)
was
used
for
morpho-
metric
analysis
of
the
mechanoreceptors.
Results
Three
morphologically
distinct
mechanore-
ceptors
were
identified
both
in
the
MGHL
as
well
as
in
LGHL:
Ruffini
receptors
or
type
I
endings
(Fig.
1),
Pacinian
corpuscles
or
type
II
endings
(Fig.
2)
and
Golgi
tendon
organ-like
receptors
or
type
III
endings
(Fig.
3);
in
addition,
free
nerve
endings
or
type
IV
endings
(Fig.
4)
were
observed.
Ruffini
receptors
(type
I
endings)
These
mechanoreceptors,
globular
or
fusi-
form
in
shape,
appeared
singly
or
in
small
clusters
of
two
to
four
end-organs.
They
were
mainly
found
in
the
deeper
layers
of
the
ligaments.
Each
nerve
ending
consisted
of
a
nerve
fiber
branched
in
a
dense
terminal
arborisation
wrapped
in
a
thin
capsule.
The
size
of
these
receptors
was
variable,
ranging
from
46
to
173
gm
in
length,
and
30
to
95
gm
in
width
(average
dimension:
115
x
58
gm).
I
ff.
(a)
Pacinian
corpuscle
in
MGHL
(a)
and
LGHL
(b).
Bar
=
100
gm.
Gold
chloride.
Vet
Comp
Orthop
Traumatol
4/2007
293
Mechanoreceptors
in
canine
glenohumeral
ligaments
14.
Golgi
tendon
organ
-
like
receptor
in
LGHL.
Bar
=
200
gm.
Gold
chloride.
Free
nerve
endings
in
MGHL.
Bar
=
100
gm.
Gold
chloride.
In
the
MGHL,
there
were
1-16
type
I
endings
per
specimen
(mean+SD:
7.6+5.9),
which
accounted
for
51+19%
of
all
of
the
mechanoreceptors,
whereas
in
the
LGHL
there
were
1-5
type
I
endings
per
specimen
(mean+SD:
3+1.3),
which
made
up
46+12%
of
all
of
the
mechanoreceptors.
Pacinian
corpuscles
(type
II
endings)
These
nerve
endings
were
ellipsoidal
cor-
puscles
which
averaged
250
gm
in
length
and
45
gm
in
width.
Each
one
consisted
of
a
thinly
encapsulated
non-branching
terminal
nerve
fibre.
The
single
axon
within
the
cap-
sule
was
often
slightly
expanded
and
ter-
minated
near
the
tip
of
the
corpuscle.
Paci-
nian
corpuscles
were
prevalently
observed
on
the
superficial
layer
of
the
ligaments
and
they
were
oriented
parallel
to
the
bundles
of
the
collagen
fibres.
In
the
MGHL,
there
were
1-5
type
II
endings
per
specimen
(mean+SD:
2.6+1.7),
which
accounted
for
21+7%
of
all
mech-
anoreceptors,
whereas
in
the
LGHL
there
were
0-3
type
II
endings
per
specimen
(mean+SD:
1.4+1.1),
which
made
up
22+16%
of
all
of
the
mechanoreceptors.
Golgi
tendon
organ-like
receptors
(type
Ill
endings)
These
mechanoreceptors
were
large
struc-
tures
that
measured
approximately
1000
gm
in
length
and
75
gm
in
width.
They
were
in-
nervated
by
a
large
afferent
fibre
which
bi-
furcated
into
diverging
branches.
Each
branch
entered
a
thin
capsule
and
gave
off
a
dense
arborisation
which
showed
multiple
small
globular
expansions.
The
long
axis
of
these
mechanoreceptors
was
found
in
the
long
axis
of
the
ligament
and,
due
to
their
di-
mensions,
they
occupied
almost
all
the
thickness
of
the
ligaments
themselves.
In
the
MGHL,
there
were
1-5
type
III
endings
per
specimen
(mean+SD:
2.9+1.5),
which
accounted
for
29+17%
of
all
mech-
anoreceptors,
whereas
in
the
LGHL
there
were
1-2
type
III
endings
per
specimen
(mean+SD:
1.8+0.4),
making
up
35+17%
of
all
of
the
mechanoreceptors.
Distribution
of
mechanoreceptors
in
the
ligaments
The
MGHL
and
LGHL
were
divided
into
thirds
along
the
proximo-distal
direction
(glenoid,
central
and
humeral
portions)
and
the
number
of
mechanoreceptors
of
each
type
was
compared.
In
both
ligaments,
all
of
the
receptors
were
mainly
localized
at
each
end
of
the
ligaments
and
prevalently
in
the
glenoid
portion.
In
particular,
in
the
MGHL,
the
percentage
of
type
I
endings
in
the
gle-
noid,
central
and
humeral
portions
was
81+16%
(mean+SD%),
8+11%
and
11+12%,
respectively;
the
percentage
of
type
II
endings
in
the
same
portions
was
84+22%,
7+19%
and
9+16%,
respectively;
and
the
percentage
of
type
III
endings
was
55+42%,
3+8%
and
42+43%,
respectively.
Furthermore,
in
the
glenoid
portion
of
the
MGHL,
type
I,
type
II
and
type
III
endings
were
most
commonly
found
in
the
cranial
branch
of
the
insertion
into
the
scapula,
with
this
portion
accounting
for
88+15%,
73+35%
and
55+30%,
respectively,
and
in
the
caudal
branch,
with
12+15%,
27+35%
and
45+30%,
respectively.
In
the
LGHL,
the
percentage
of
type
I
endings
in
the
glenoid,
central
and
humeral
portion
was
57+33%,
19+24%
and
24+27%,
respectively,
whereas
the
percen-
tage
of
type
II
endings
was
63+22%,
17+24%
and
20+27%,
respectively,
and
fin-
ally,
the
percentage
of
type
III
endings
was
64+24%,
0+0%
and
36+24%,
respectively.
Discussion
To
our
knowledge,
this
study
is
the
first
in-
vestigation
about
the
types
and
the
topogra-
phy
of
mechanoreceptors
in
the
MGHL
and
LGHL
of
dogs.
In
this
study,
three
types
of
specialized
receptors
were
found:
Ruffini
receptors,
Pacinian
corpuscles
and
Golgi
tendon
organ-like
receptors,
and
in
addition,
free
nerve
endings
were
also
observed.
This
is
in
agreement
with
studies
by
other
authors
on
human
shoulder
joints
(26,
28,
29),
mouse
shoulder
joints
(30)
and
feline
shoulder
joint
capsules
(12),
and
limited
to
type
I
and
type
II
endings
in
Monodelphis
Vet
Comp
Orthop
Traumatol
4/2007
294
Grandis
et
al.
domestica
shoulder
joint
(31).
The
most
abundant
mechanoreceptors
found
in
dog
shoulder
ligaments
were
Ruffini
receptors,
followed
by
Golgi
tendon
organ-like
recep-
tors
and
Pacinian
corpuscles.
Our
observa-
tions
are
generally
consistent
with
those
of
Guanche
et
al.
(29)
and
Steinbeck
et
al.
(32)
who
described
the
Ruffini
endings
as
the
most
common
found
in
human
glenohum-
eral
ligaments.
On
the
contrary,
our
data
are
different
from
the
findings
in
the
mouse
(30)
and
Monodelphis
domestica
(31)
shoulder
joint
region
in
which
the
Pacinian
corpuscles
were
more
abundant
and
the
Ruffini
receptors
were
identified
only
in
small
numbers.
With
regard
to
the
localization
and
dis-
tribution,
the
present
study
shows
that
most
of
the
mechanoreceptors
were
located
in
the
glenoid
portion
of
the
ligaments
and,
in
par-
ticular,
that
the
highest
density
was
at
the
cranial
arm
of
the
MGHL.
Previous
investi-
gations,
in
mouse
(30)
and
Monodelphis
do-
mestica
(31)
shoulder
joints,
likewise
re-
ported
that
a
large
number
of
mechanore-
ceptors
were
located
close
to
the
glenoid
la-
brum.
In
contrast,
in
human
inferior
gleno-
humeral
ligaments,
Ruffini
endings
were
found
close
to
the
insertion
on
the
humerus
(32).
The
different
distribution
between
ca-
nine
and
human
models
was
predictable
since
the
function
of
the
canine
shoulder
joint
differs
considerably
from
the
function
of
the
human
shoulder
joint,
for
example,
the
canine
shoulder
carries
a
part
of
the
body
weight.
The
variety
of
mechanoreceptors
in
ca-
nine
shoulder
ligaments
might
indicate
an
afferent
function
in
providing
the
CNS
with
joint
proprioceptive
information.
These
specialized
nerve
endings
most
likely
play
an
important
role
in
the
control
of
shoulder
joint
movement
and
stability.
In
fact,
as
demonstrated
experimentally
in
the
cat,
a
spinal
reflex
exists
between
the
capsulo-
ligamentous
structures
and
the
muscles
around
the
shoulder
(10-12).
Afferent
pro-
prioceptive
information
arising
from
the
mechanoreceptors,
which
are
located
in
the
capsulo-ligamentous
structures,
travels
via
the
articular
nerves
to
the
spinal
cord.
The
afferent
neurons
may
synapse
directly
with
the
alpha
or
gamma
motor
neurons
which
innervate
periarticular
muscles
or
indirectly
with
interneurons
(16,
32).
Although
there
are
many
studies
concerning
the
joint
func-
tions
of
specialized
nerve
endings,
the
role
of
this
reflex
arc
has
not
yet
been
clarified.
Early
studies
that
demonstrated
the
exist-
ence
of
a
reflex
arc
from
the
glenohumeral
capsule
to
the
cuff
muscles,
in
anaesthetized
cats,
showed
that
a
stimulation
of
the
articu-
lar
branches
of
the
axillary,
musculocu-
taneous,
suprascapularis
and
subscapularis
nerves
elicited
electromyographic
activity
in
several
muscles
(biceps,
subscapularis,
supraspinatus,
infraspinatus
and
deltoid)
(10-12).
The
average
latency
of
the
muscu-
lar
response
to
stimulation
of
the
joint
cap-
sule
was
3
msec,
which
was
fast
enough
to
be
joint
protective
(10).
The
increase
of
peri-
articular
muscle
stiffness
results
in
en-
hanced
joint
stiffness
and,
therefore,
an
aug-
mentation
of
its
stability
(16).
Recently,
Diederichsen
et
al.
(34)
carried
out
a
study
in
order
to
determine
the
effect
of
low
am-
plitude
electrical
stimulation
applied
to
the
coracoacromial
ligament
(CAL)
on
the
ac-
tivity
of
shoulder
muscles
during
isometric
extension
or
flexion
in
conscious
healthy
humans.
They
demonstrated
a
general
in-
hibition
of
the
voluntarily
activated
shoulder
muscles
when
the
CAL
was
stimu-
lated,
with
latencies
ranging
from
60
to
80
msec.
These
findings
do
not
support
the
hy-
pothesis
of
joint
protective
muscle
reflexes
but
they
do
put
forward
the
notion
that these
reflexes
may
contribute
to
muscle
coor-
dination
and
joint
stability
through
a
feed-
forward
mechanism.
Such
results
have
pre-
viously
been
shown
in
the
human
shoulder
after
non-noxious
stimulation
of
the
gleno-
humeral
joint
capsule
in
conscious
subjects
(35).
All
of
these
data
led
us
to
hypothesize
that
in
the
dog,
as
in
man
and
in
cats,
in
ad-
dition
to
acting
as
passive
mechanical
stabi-
lizers,
glenohumeral
ligaments
may
serve
as
a
sensory
structure
by
means
of
the
mech-
anoreceptors
embedded
within
them,
con-
tributing
actively
to
joint
stability.
The
mechanoreceptors
that
are
involved
in
the
spinal
reflex
possess
different
physio-
logical
characteristics
and
functions;
Ruffi-
ni
and
Golgi
tendon
organ-like
receptors
adapt
slowly
to
movements,
and
identify
motion
and
position
of
the
ligament,
thus
allowing
the
CNS
to
interpret
the
position
and
the
angle
of
rotation
of
the
joint,
where-
as
Pacinian
corpuscles,
which
adapt
rapidly
to
movements,
can
detect
the
acceleration
and
deceleration
applied
to
the
ligament
at
the
beginning
and
the
end
of
the
movement
(26-28,
36).
Free
nerve
endings
act
as
pain
receptors,
and
also
have
a
vasomotor
action
(27).
The
presence
of
a
greater
number
of
slowly
adapting
receptors
with
regard
to
quickly
adapting
receptors,
suggests
that
the
sensation
of
position
and
movement
of
the
ligaments
plays
a
more
important
role
than
the
changes
of
velocity
in
the
kinetics
of
the
shoulder
joint.
This
hypothesis
must
be
con-
firmed
by
additional
studies
on
shoulder
kinetics
but
it
could
be
explained
when
one
considers
that,
whilst
the
chief
movements
of
the
canine
shoulder
are
flexion
and
exten-
sion
(37);
this
joint
can
move
in
any
direc-
tion
and
the
proprioceptive
neural
input
from
the
shoulder
requires
a
large
number
of
receptors
in
order
to
continuously
identify
the
position
and
the
angle
of
rotation
of
the
joint.
Moreover,
our
study
showed
that
the
highest
density
of
these
receptors
was
at
the
cranial
arm
of
the
glenoid
portion
of
the
MGHL.
These
observations
led
us
to
hypo-
thesize
that
this
end
of
this
ligament
is
the
most
sensitive
site,
the
one
which
receives
the
major
part
of
the
mechanical
stimuli.
These
data
could
explain
the
large
propor-
tion
of
medial
shoulder
instability
(75%)
as-
sociated
with
an
abnormal
MGHL
(19).
Furthermore,
these
findings
may
have
some
clinical
implications.
We
can
hypo-
thesize
that ligamentous
injuries
that
occur
in
the
shoulder
from
traumas
or
surgical
procedures
not
only
affect
mechanical
re-
straint
but,
because
of
the
disruption
of
the
mechanoreceptors,
they
can
also
alter
the
proprioceptive
input
to
the
CNS.
For
this
reason,
surgeons
who
perform
shrinking
or
capsular
shifts
which
involve
capsuloliga-
mentous structures
in
arthroscopic
or
open
surgical
procedures
must
take
these
effects
into
account
and,
when
possible,
they
should
avoid
the
mechanoreceptor-dense
regions.
However,
it
has
been
demonstrated
that,
in
the
rabbit,
the
mechanoreceptors
re-
generated
after
anterior
cruciate
ligament
reconstruction
using
a
free
bone-patellar
tendon-bone
graft
and,
at
eight
weeks
post-
operatively,
the
number
of
receptors
was
not
significantly
different
in
the
control
nor
in
Vet
Comp
Orthop
Traumatol
4/2007
295
Mechanoreceptors
in
canine
glenohumeral
ligaments
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Correspondence
to:
Annamaria
Grandis
DVM
Dept.
of
Veterinary
Morphophysiology
and
Animal
Productions
University
of
Bologna,
Via
Tolara
di
Sopra,
50
Ozzano
dell'Emilia,
Bologna
40064,
Italy
Phone:
+39
512097939,
Fax
+39
512097953
E-mail:
Vet
Comp
Orthop
Traumatol
4/2007