the fine structure of the purkinje cell
TRANSCRIPT
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T H E F I N E S T R U T U R E O F
T H E P U R K I N J E E L L
R O B E R T M . H E R N D O N , M . D .
F r o m t h e D e p a r t m e n t o f P a t h o lo g y a n d D e p a r t m e n t o f N e u r o l o g y a n d N e u r o s u rg e r y , M c G i l l
Un i v e rs i t y a n d t h e M o n t re a l Ne u ro l o g i c a l In s t i t u t e , M o n t re a l , C a n a d a
A B S T R A C T
T h i s p a p e r d e s c r i b e s t h e f i n e s t r u c t u r e o f t h e P u r k i n j e c e l l o f t h e r a t c e r e b e l l u m a f t e r f i x a t io n
b y p e r f u s io n w i t h 1 p e r c e n t b u f f e r e d o s m i u m t e t r o x id c . S t r u c t u r e s d e s c r i b e d i n c l u d e a
l a r g e G o l g i a p p a r a t u s , a b u n d a n t N i ss l s u b s t a n ce , m i t o c h o n d r i a , m u l t i v e s i c u l a r bo d ie s ,
o s m i o p h i l i c g r a n u l e s , a x o d e n d r i t i c a n d a x o s o m a t i c s yn a p s e s , th e n u c l e u s , th e n u c l e o l u s , a n d
t h e n u c l e o l a r b o d y. A n e w a n d p o s s ib l y u n i q u e r e l a t io n s h i p b e t w e e n m i t o c h o n d r i a a n d
s u b s u r f a c e c i s t e rn s i s d e s c r i h c d . P o s s i b l e f u n c t i o n a l c o r r e l a t i o n s a r e d i s c u s se d .
T h e l a r g e , u n i f o r m n e u r o n s , w h i c h a r e n a m e d a f t e r
t h e C z e c h p h y s i o l o g i s t w h o f i r st d e s c r i b e d t h e m ,
f o r m t h e s o l e o u t p u t p a t h w a y o f t h e c e r e b e l l a r
c o r t e x a n d , a s s u c h , a r e a n e s s e n t i a l l in k i n a
c o m p l e x f e e d b a c k s y st e m w h i c h a c t s o n t h e m o t o r
s y s te m o f t h e b o d y t o r e g u l a t e m u s c l e t o n e a n d
m o v e m e n t . T h e f u n c t i o n a l i m p o r t a n c e o f t h e se
c e ll s a n d t h e i r m a r k e d v u l n e r a b i l i t y t o c e r t a in
t o x i c co n d i t i o n s m a k e s t h e m o f p a r t i c u l a r i n t e r e s t
t o t h e n e u r o l o g i s t a n d n e u r o p a t h o l o g i s t .
K n o w l e d g e o f th e s t r u c t u r e o f t h e s e c e ll s
b e g a n w i t h P u r k i n j e w h o d e s c r i b e d t h e m i n a
p a p e r o n t h e h i s t o lo g y o f th e n e r v o u s s y s t e m
p r e s e n t e d i n P r a g u e i n 1 8 3 7 ( F i g . 1 ) .
J e d e s d i e s e r K 6 r p e r c h e n i s t m i t d e m s t u m p f e n ,
r u n d l i c h e n E n d e n a c h I n n e n g e g e n d i e g e l b e
S u b s t a n z g e k e h r t , u n d z e i g t i n s e i n em K o l b e n
d e u t l i c h s a m m t s e i n e m H o l e d e n c e n t r a l e n K e r n ;
d a s a n d e r e s c h w a n z f 6 r m i g e E n d e i s t n a c h A u s s e n
g e r i c h t e t , u n d v e r l i e r t s i c h rn i t me i s t z we i e n Fo r t -
s / i t z e n i n d e r g ra u e n Su b s t a n z b i s n a h e a n d i e a u s -
se re Pe r i p h e r i e wo d i e se mi t d e r Ge f~ i s sh a u t u msp o n -
n e n i s t . 1
J o h a n n e s E v a n g e l i s te P u r k i n j e ( 3 9) .
1 E a c h o n e o f th e s e b o d ie s is t u r n e d w i t h t h e b l u n t
r o u n d e d e n d i n w a r d t o w a r d s t h e y e l lo w s u bs t a n ce ,
a n d c l e a r l y sh o ws i n i t s b o d y t h e n u c l e u s a s we l l a s
i t s h a l o ; t h e o t h e r t a i l - sh a p e d e n d i s d i re c t e d o u t wa rd
I n t h e c e n t u r y a n d a q u a r t e r s i n c e h e d e s c r i b e d
t h e m , c o n s i d e r a b l e d e t a i l ha s b e e n a d d e d t o
k n o w l e d g e o f t h e i r s t r u c tu r e . W i t h G o l g i ' s di s-
c o v e r y o f a m e t h o d f o r s el e c ti v e i m p r e g n a t i o n o f
n e u r o n s b y s i l v e r s a l ts , i n 1 87 0, i t b e c a m e p o s s i b l e
t o t r a c e t h e c e l l p r o c e s se s o f i n d i v i d u a l c e l ls f o r
l o n g d i s t a n c e s ( 1 2 ). U s i n g t h is t e c h n i q u e , h e
o b s e r v e d a n d d e s c r i b e d t h e e x t e n s i v e d e n d r i ti c
r a m i f i c a t io n s o f t h e P u r k i n j e c e l l, a n d t r a c e d
t h e i r a x o n s a n d c o l l a t e r a l s ( 1 3 ) . I n d o i n g s o , h e
e l u c i d a t e d m a n y o f th e c e l l u l a r r e l a ti o n s h ip s i n
t h e c e r e b e ll u m . R a m 6 n y C a ja l , w h o r e f i ne d
G o l g i ' s t e c h n i q u e s a n d d e v e l o p e d a n u m b e r o f
h is o w n , a d d e d m u c h t o o u r k n o w l e d g e o f t h e
P u r k i n j e c e l l a n d i t s r e l a t i o n s h i p s . H e d e m o n -
s t r a t e d t h e d e n d r i t i c s p i n e s , t h e a x o s o m a t i c , a x o -
d e n d r i t i c a n d t h e a x o - a x o n i c s y na p s e s o f t h e
P u r k i n j e c e l l , a n d t h e r e c u r r e n t a x o n c o l l a t e r a l s
w h i c h s y n a p s e o n a d j a c e n t P u r k i n j e c e l l s . H e a l s o
d i s c o v e r e d t h e b a s k e t c e ll s a n d g r a n u l e c e l l
a x o n s ( 4 0 - 4 3 ) .
F r a n z N i s s l ( 2 6 ) d e s c r i b e d t h e m a t e r i a l , w h i c h
b e a r s h is n a m e , i n a n u m b e r o f d i f f e r e n t n e r v e
c e l ls i n c l u d i n g t h e P u r k i n j e c e l l i n 1 8 94 , a n d o v e r
t h e f o l l o w i n g y e a r s i ts i m p o r t a n c e i n r e g a r d t o
a n d l ose s i ts e l f wi t h u su a l l y t w o p ro c e sses i n t h e g re y
su b s t a n c e c l o se t o t h e p e r i p h e ry , wh e re t h i s i s i n -
v e s t e d b y t h e v a s c u l a r m e m b r a n e .
167
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cel lu l ar pa thology was f i rmly es t abl i shed. I t s
e q u i v a l e n c e w i t h t h e g r a n u l a r e n d o p l a s m i c
r e t i c u l u m o f e l e c tr o n m i c r o s c o p y w a s d e m o n -
s t r a t e d b y P a l a y a n d P a l a d e i n a c o m p a r a t i v e
l ight and e l ec t ron microscopic s tudy publ i shed
in 1955 (36).
In 1898, Golgi , us ing a new s ta in ing me thod
(14) , descr ibed and i l l us t r a t ed a r e t i cular ne twork
wi th in the cytoplasm of the Purkin j e ce l l of t he
Thi s v i ew, however , has been ques t ioned r ecent ly
on th e bas is of s tudies on the Purk inje cel ls of
owls (24) ; this point wi l l be discussed later .
C y t o p l a s m i c g r a n u l e s a p p a r e n t l y d i s t i n c t f r o m
both Ni s sl subs t ance and Golgi appara tus have
al so been descr ibed in the Purkin j e ce l l ( 2 , 21 ,
4 7 4 9 ) .
The num erous con nect ions of t he Purkin j e ce l l
were emphas i zed by Fox (10) who ca l cula t ed
FIGURE 1
This plate is taken f rom Purkinje s descr ipt ion of
the cerebcl lar cor tex and shows, f rom top to bot-
tom, the molecular layer , the Purkinje cel l layer ,
the granu le cel l layer , and the white ma t ter (39).
owl , Strix flammea (Fig . 2) . Thi s ne twork, which
could be s een only wi th specia l f i xa t ion and
s t a in ing t echniques , was cons idered by many to
be an ar t i f ac t (29) . Wi th the fur ther appl i ca t ion
of the e l ec t ron microscope to b io logica l mater i a l s ,
t h e e q u i v a l e n c e o f t h e G o l g i a p p a r a t u s o f li g h t
m i c r o s c o p y w i t h t h e a g r a n u l a r r e t i c u l u m o f
e l ec t ron microscopy was demons t r a t ed (3 , 4) .
FIGURE
This drawing by Golgi i l lus t rates the network
which bears his nam e in the Purkinje cel l of the
owl, Strixflammea (14).
t ha t t here ar e about 61 ,000 dendr i t i c sp ines on a
s ingle dend r i t e and tha t t here ar e f rom 223,000
to 297,000 para l l e l f i br es pas s ing through the
dendr i t i c spread of a s ingle Purkin j e ce l l . More
recent , e l ec t ron microscopic observat ions by Fox
(11) and by Gray (18) have conf i rme d the synapt i c
nature of t he dendr i t i c sp ines and e lucida t ed the i r
f ine s t ructure.
Many fur ther observat ions on the f ine s t ructure
of nerve ce l l s , i nc luding Purkin j e ce l l s , have been
FIGURE 3
In this low power micrograph of a Purkinje cel l , the dendr i te (d) is readi ly seen at the
uppe r r ight . Th e or igin of the axon (a) , cut at an angle, i s seen at the bot tom. T he
agranu lar membran es and ves icles of the Go lgi apparatus (out l ined) can be seen
around the nucleus and in the base of the dend r i te (compare w ith Fig. 2). Mitoc hond ria
and dense granules can be seen scat tered throu ghout the cytoplasm along with nu-
merous elements of granu lar endo plasmic ret iculum. Several mitoch ondria in close
association with subsurface cisterns are also seen (arrows).
A smal l per icel lular space can b e seen in some areas . This is ar ti fact caused by shr ink-
age and is not a true pericellular space. X 6,400.
168 THE JOURNAL OF CELL BIOLOGY VOLUME 18 1968
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ROBERT M. I Iv.RNDON Fine Structure of Purt~inje ell 169
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m a d e 1 , 7, 9 , 2 3 , 3 0 , 3 3 ) ; h o w e v e r , a n a d e q u a t e
e l e c t r o n m i c r o s c o p i c s t u d y o f t h e P u r k i n j e c e l l
w a s n o t p o s s i b le u n t i l t h e a d v e n t o f f i x a t i o n b y
p e r f u s i o n w i t h s o l u ti o n s o f o s m i u m t e t r o x i d e 3 7 ) .
T h e o b j e c t o f th i s p a p e r i s t o g i v e a s y s t e m a t i c
a c c o u n t o f t h e P u r k i n j e c e l l o f th e r a t a s it a p p e a r s
i n t h e e l e c t r o n m i c r o s c o p e a f t e r p e r f u s i o n f i x a t i o n
w i t h b u f f e r e d o s m i u m t e t r o x i d e . T h i s w i l l p r o v i d e
a b a s e l i n e fo r t h e s t u d y o f e x p e r i m e n t a l l y i n d u c e d
c h a n g e s a n d a l so m a y p r o v i d e s o m e b a s i s f o r
c o r r e l a t i o n o f s t r u c t u r e w i t h f u n c t i o n .
M A T E R I A L S A N D M E T H O D S
R a t s w e i g h i n g f r o m 2 0 0 t o 3 0 0 g r a m s w e r e a n e s -
t h e t i z e d w i t h i n t r a p e r i t o n e a l p e n t o b a r b i t a l . F i x a t i o n
w a s c a r r i e d o u t b y t h e p e r f u s i o n m e t h o d o f P a l a y
3 7 ) w i t h t h e m i n o r m o d i f i c a t i o n t h a t t h e c a n n u l a
w a s p l a c e d i n t h e d e s c e n d i n g a o r t a p o i n t i n g i n a
c r a n i a l d i r e c t i o n a n d t h e p r o x i m a l a o r t a w a s l i g a t e d .
W h e n f i x a t i o n w a s s u c ce s s fu l , t h e e n t i r e c e r e b r u m a n d
c e r e b e l l u m w e r e b l a c k e n e d s a v e f o r a f e w s m a l l
a r e a s . T h e f i x a t i v e u s e d w a s a c e t a t e v e r o n a l b u f f e r e d
1 p e r c e n t o s m i u m t e t r o x i d e w i t h s a l ts a d d e d , a s
d e s c r i b e d b y Z e t t e r q v i s t 5 2 ) , a n d c a l c i u m c h l o r i d e
a d d e d t o b r i n g t h e s o l u t i o n t o a f i n a l c a l c i u m c o n -
c e n t r a t i o n o f 5 . 4 m g o f c a l c i u m p e r m l o f so l u t i o n .
W e h a v e f o u n d f i x a t i o n w i t h t h i s m e t h o d s u p e r i o r
t o i m m e r s i o n f i x a t i o n a n d a l s o t o f i x a t i o n b y p e r -
f u s i o n w i t h c o l d s o l u t i o n s o f o s m i u m t e t r o x i d e . O b -
s e r v a t i o n s w e r e m a d e o n f o u r r a t s p e r f u s e d i n t h i s
f a s h i o n a l o n g w i t h s o m e o b s e r v a t i o n s m a d e o n t i s s u e
f i x e d b y i m m e r s i o n a n d t i s s u e f i x e d b y p e r f u s i o n
w i t h b u f f e r e d 2 p e r c e n t p e r m a n g a n a t e s o l u t i o n .
T h e l a t t e r p e r fu s i o n m e t h o d , w h i c h w a s p e r f o r m e d
o n f i v e r a t s , wa s f o u n d t o b e l e s s sa t i s f a c to r y a n d
t e c h n i c a l l y m o r e d i f f i c u l t t h a n p e r f u s i o n w i t h s o l u -
t i o n s o f o s m i u m t e t r o x i d e . F o r t y m i n u t e s a f t e r t h e
s t a r t o f t h e p e r f u s i o n , t h e c e r e b e l l u m w a s r e m o v e d
a n d b l o ck s w e re c u t i n a m a n n e r w h i c h a l l o w e d f or
e m b e d d i n g i n t h e d e s ir e d p l a n e . T h e b l o ck s w e r e
t h e n d e h y d r a t e d t h r o u g h a g r a d e d s e ri es o f e t h y l
a l c o h o l f o l l o w e d b y p r o p y l e n e o x i d e a n d e m b e d d e d
i n E p o n 8 1 2 2 2 ) . A f t e r p o l y m e r i z a t i o n t h e b l o c k s
w e r e t r i m m e d a n d s e c t i o n e d o n a P o r t e r - B l u m m i c r o -
t o m e w i t h a g l a s s k n i f e . T h e s e c t i o n s w e r e p i c k e d u p
o n c o p p e r g r i d s c o a t e d w i t h f o r m v a r a n d c a r b o n ,
s t a i n e d w i t h a l k a l i n e l e a d a c e t a t e 3 8 , 5 0 ) , a n d e x -
a m i n e d w i t h a n R C A E M U 3 E e le c t r o n m i c r o sc o p e .
A d j a c e n t t h i c k s e c t i o n s w e r e e x a m i n e d w i t h t h e
p h a s e c o n t r a s t m i c r o s c o p e .
O B S E R V A T I O N S
I n t h e e l e c t r o n m i c r o s c o p e , a s i n l i g h t m i c r o s c o p y ,
t h e P u r k i n j e c e l l s a r e l a r g e c e ll s w i t h a d i a m e t e r
o f 2 5 t o 4 0 m i c r o n s F i g . 3 ) s i t u a t e d b e t w e e n t h e
g r a n u l e c e l l l a y e r a n d t h e m o l e c u l a r l a y e r o f t h e
c e r e b e l lu m . T h e i r d e n d r i t e s a r b o r i z e i n a p l a n e
a t r i g h t a n g l e s t o t h e c e r e b e l l a r f ol i a, a n d t h e
t e r t i a r y d e n d r i t e s a r e s t u d d e d w i t h d e n d r i t i c
s p in e s . U n l i k e t h e a r r a n g e m e n t i n m a n y n e u r o n s ,
t h e P u r k i n j e c e l l a x o n t a k e s o f f d i r e c t l y f r o m t h e
c e l l b o d y w i t h n o a x o n h i l l o c k . I n t h e e l e c t r o n
m i c r o s c o p e , p r o p e r l y o r i e n t e d s e c t i o n s s h o w t h e
P u r k i n j e c e l l d e n d r i t e s a s t h e y d i v i d e a n d r e d i v i d e
i n t h e m o l e c u l a r l a y e r F i g . 5 ) . N u m e r o u s m i t o -
c h o n d r i a a n d e l e m e n t s of g r a n u l a r e n d o p l a s m i c
r e t i c u l u m c a n b e s e e n in t h e p e r i p h e r a l p o r t i o n
o f t h e l a r g e r d e n d r i t e s , a n d d e n d r i t i c c a n a l i c u l i
1 7 , 3 3 , 3 7 ) a r e r e g u l a r l y a r r a n g e d t h r o u g h o u t
t h e d e n d r i t e s. T h e t e r t i a r y b r a n c h e s o f t h e
d e n d r i t e s c o n t a i n f e w c a n a l i c u l i a n d t h e m i t o -
c h o n d r i a a r e e l o n g a t e d w i t h t h e i r c r i s t ae u s u a l l y
r u n n i n g p a r a l l e l t o th e i r l o n g a xi s . T h e s e t e r t i a r y
b r a n c h e s a r e s t u d d e d w i t h s m a l l p r o j e ct i o n s w h i c h
u s u a l l y m a k e o n e s y n a p t i c c o n n e c t i o n a n d c a n
r e a d i l y b e s e e n t o b e e q u i v a l e n t t o t h e d e n d r i t i c
s p i n e s s e e n w i t h t h e l i g h t m i c r o s c o p e .
T h e i n i t i a l s e g m e n t o f P u r k i n j e c e l l a x o n i s
u n m y e l i n a t e d b u t t h e r e m a i n d e r o f t h e a x o n is
h e a v i l y m y e l i n a t e d . W i t h i n t h e a x o n a r e a
m o d e r a t e n u m b e r o f c a n a l i cu l i , m i t o c h o n d r i a ,
a n d s c a t t e r e d v e s i c le s r a n g i n g i n s iz e f r o m a b o u t
5 0 t o 1 5 0 m ~ .
T h r e e t y p es o f s y n a p s e a r e s e e n o n t h e P u r k i n j e
c e ll . T h e f i r s t t y p e t y p e 1 o f G r a y ) i s t h e a x o d e n -
d r i t i c s y n a p s e F i g . 6 ) w h i c h i s c o m p o s e d o f a
t e r m i n a l b o u t o n a n d a d e n d r i t i c s p i n e . T h i s
b o u t o n c o n si s ts o f a t e r m i n a l a x o n a l e n l a r g e m e n t
c o n t a i n in g o n e o r m o r e m i t o c h o n d r i a a n d s y n a p -
t i c v e si c le s . T h e p r e - a n d p o s t s y n a p t i c m e m b r a n e s
a r e s e p a r a t e d b y a b o u t 3 0 0 A n g s t r o m s a n d w i t h i n
t h e s y n a p t i c c l e f t i s a t h i n d e n s e l i n e . T h e p o s t -
s y n a p t i c m e m b r a n e , u n l i k e t h a t in t h e a x o -
s o m a t i c s y n a p s e , i s u s u a l l y c o n s i d e r a b l y t h i c k e n e d
r e l a t i v e t o o t h e r p o r t i o n s o f t h e P u r k i n j e c e l l
m e m b r a n e . T h e s p in e a p p a r a t u s w h i c h i s f re -
q u e n t l y s e e n i n d e n d r i t i c s p i n e s i n t h e c e r e b r a l
c o r t e x 1 6 , 1 7 ) h a s n o t b e e n f o u n d i n t h e s p i n e s
o f t h e P u r k i n j e c e ll . T h e s e c o n d t y p e t y p e 2 o f
G r a y ) 1 6 - 1 9 ) is t h e a x o s o m a t i c s y n a p s e F i g . 7 )
w h i c h c o n s i s ts , a s i n t h e c a s e o f t h e a x o d e n d r i t i c
s y n a p se , o f a t e r m i n a l e x p a n s i o n o r b o u t o n
c o n t a i n i n g n u m e r o u s s y n a p t i c v e si cl es a n d u s u a l l y
o n e o r m o r e m i t o c h o n d r i a . O n e s i de o f t h i s b o u t o n
i s c l o s el y a p p l i e d t o t h e c e l l b o d y , a n d t h e s y n a p t i c
v e s ic l e s a r e m o r e d e n s e l y p a c k e d a l o n g t h i s r e g i o n
o f c lo s e c o n t a c t. T h e p r e - a n d p o s t s y n a p ti c m e m -
1 7 0 T HE JOURNAL OF CE L L B IOL OGY VOL UME 1 8 1 9 6 3
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FIGURE
This composite drawing of a Purkinje cell illustrates many of the structures described in this paper.
The axon is seen at the lower right and the dendrite is at the top. Also shown are axosomatic syn-
apses, subsurface cisterns ssc) with associated mitochondria, the Golgi apparatus, multivesicular
bodies mvb), endoplasmic reticulum er), and dense bodies db). In the nucleus, the nucleolus and
nucleolar body nb) are easily seen. Neural tubules can be seen concentrated in the dendrite and
axon. Drawing by Miss E. Sweczey.
branes are separated by a space of 180 to 200
Angstroms. The structure of the axo-axonic
synapse has not been worked out in detail. These
latter synapses are located on the proximal,
unmyelinated, portion of the Purkinje cell axon.
Beneath the cell membrane of the body of the
cell, narrow membrane-bounded cisterns similar
to those described by Rosenbluth in cells of the
acoustic ganglion are frequently seen 45, 46).
Each subsurface cistern has, in most instances, a
ROBERT M. HERNDON Fine Structure of Purkinje Cell 171
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m i t o c h o n d r i o n c l o s e l y a p p l i e d t o i ts i n n e r s u r f a c e
( F i g . 8 ) . I n m o s t i n s t a n c e s , t h e m i t o c h o n d r i o n
a p p e a r s t o c o v e r v i r t u a l l y t h e e n t i r e i n n e r s u r f a c e
o f t h e c is t e r n . S u b s u r f a c e c i s t e r n s w i t h o u t a s s o -
c i a t e d m i t o c h o n d r i a w e r e a ls o o c c a s i o n al l y s ee n
i n t h e s e c e l l s . I n s o m e i n s t a n c e s , t h e r e a p p e a r e d
t o b e c o n t i n u i t y b e t w e e n t h e s u b s u r f a c e c i s t e r n s
a n d t h e e n d o p l a s m i c r e ti c u l u m . I n a n u m b e r o f
i n s t a n c e s, t h e r e a p p e a r e d t o b e o n e o r t w o r i n g -
l i k e s t ru c t u re s , p o ss i b l y v e s i c l e s o r , m o re l i k e l y ,
c r o s s - s e c t io n e d t u b u l e s , a t o n e e n d o f a s u b s u r f a c e
c i s t e r n . T h e s u b s u r f a c e c i s t e r n s d o n o t a p p e a r t o
b e a r a n y c o n s t a n t r e l a t i o n s h i p w i t h a n y e x t r a -
c e l l u l a r s t r u c t u r e .
S c a t t e r e d t h r o u g h o u t t h e c y t o p la s m a n d i n th e
m a j o r d e n d r i t i c b r a n c h e s , t h e r o u g h l y p a r a l l e l
m e m b r a n e s o f t h e g r a n u l a r e n d o p l a s m i c r e t i c u l u m
c a n b e s ee n . T h e s e m e m b r a n e s h a v e , o n t h e i r
o u t e r s u r f ac e s , n u m e r o u s 1 50 A n g s t r o m d e n s e
r i b o n u c l e o p r o t e i n g r a n u l e s ( 3 1 , 3 2 ) . A d d i t i o n a l
u n a t t a c h e d R N P g r a n u l e s a p p e a r s c a t te r e d
t h r o u g h o u t t h e c y to p l a s m . P a r a l l e l a r r a y s o f
t h es e g r a n u la r m e m b r a n e s a r e c o m m o n o n l y in
t h e r e g i o n o f t h e n u c l e us , t h e m e m b r a n e s f o u n d
i n o t h e r p a r t s o f t h e c e l l b e i n g u s u a l l y i r r e g u l a r l y
sc a t t e re d (F i g s . 4 , 5 , 9 , a n d 1 0 ) .
L o c a t e d i n t h e c y t o p l a s m a b o u t t h e n u c l e u s a n d
i n t h e r e g i o n o f t h e b a s e o f th e d e n d r i t e , n u m e r o u s
a r r a y s o f c lo s e ly pa c k e d a g r a n u l a r m e m b r a n e s
w i t h a ss o c i at e d m e m b r a n e - b o u n d e d s p a ce s a n d
v a c u o l e s a r e s e e n ( F i g s . 3 , 4 , a n d 9 ) . T h e s e
s t r u c t u r e s u s u a l l y a r e a r r a n g e d i n a s e m i l u n a r o r
c i r c u l a r p a t te r n a n d h a v e b e e n s h o w n b y D a l t o n
a n d F e l i x ( 3 , 4 ) t o b e t h e G o l g i a p p a r a t u s o f l i g h t
m i c r o s c o p y . W i t h i n s o m e o f t h e G o l g i v e s ic l e s ,
d e n s e g r a n u l a r m a t e r i a l i s o c c a s i o n a ll y s ee n . T h e
G o l g i n e t w o r k i s c o n s i d e r a b ly m o r e e x t e n s iv e
t h a n t h a t i n c e l l s f r o m m o s t o t h e r t i s su e s .
S m a l l , r o u n d o r o v a l m u l t i v e s i c u l a r b o d i e s a r e
c o m m o n l y p r e s e n t a n d a r e u s u a l l y s e e n i n c l o s e
a s s o c ia t io n w i t h t h e G o l g i a p p a r a tu s . S o m e o f
t h e s e m u l t i v e s i c u l a r b o d i e s c o n t a i n v a r y i n g
a m o u n t s o f d e n s e g r a n u l a r m a t e r i a l a n d o c c a s i o n -
a l l y a m y e l i n f i g u r e . I n s o m e b o d i e s t h e d e n s e
g r a n u l a r m a t e r i a l a l m o s t c o m p l e t e l y o b s c u r es t h e
v e s i cl e s , a n d t h e s e e x a m p l e s a p p e a r t o b e a s ta g e
i n t h e d e v e l o p m e n t o f t h e d e n s e o s m i o p h i li c b o d i e s
w h i c h a r e p r e s e n t i n a l l t h e s e c e l l s ( F i g s . 4 , 8 , a n d
9 ) . T h e s e d e n s e b o d i e s a r e b o u n d e d b y a d i s t i n c t
m e m b r a n e , a n d t h e l a r g e r on e s o f t e n c o n t a i n o n e
o r m o r e v a c u o l e s . T h e v a c u o l e s a p p e a r c l e a r i n
u n s t a i n e d a n d i n l e a d - s ta i n e d m a t e r i a l , b u t a r e
m o d e r a t e l y e l e c t r o n o p a q u e i n p h o s p h o t u n g s t ic
a c i d ~ s t a i n e d m a t e r i a l .
T h e m i t o c h o n d r i a i n t h e c e l l b o d y a r e s i m i l a r
t o t h o s e s e e n in o t h e r n e u r o n s ( 5 , 2 0 ) . T h e y a r e
g e n e r a l l y s a u s a g e - s h a p e d a n d i n m o s t i n s ta n c e s
t h e c r i s t a e r u n a t r i g h t a n g l e s t o t h e l o n g a x i s .
O c c a s i o n a l i r r e g u l a r a n d b r a n c h e d f o r m s a r e
s e en . T h e m i t o c h o n d r i a i n t h e s m a l l e r d e n d r i t i c
b r a n c h e s , o n t h e o t h e r h a n d , t e n d t o b e m o r e
e l o n g a t e d a n d t h e i r c r i s t a e u s u a l l y r u n p a r a l l e l t o
t h e l o n g a x i s o f t h e m i t o c h o n d r i o n . T h e s e e l o n -
g a t e d m i t o c h o n d r i a a r e o f t e n h e lp f u l i n i d e n ti f y i n g
t h e s m a l l e r d e n d r i t i c b r a n c h e s o f t h e P u r k i n j e c e l l.
T h e n u c l e u s h a s a r o u g h l y c i r c u l a r o u t l i n e w i t h
n u m e r o u s i n d e n t a t i o n s a n d i n f o ld i n g s of t h e
n u c l e a r m e m b r a n e w h i c h c o n s is ts o f t w o e l e c t r o n
o p a q u e p a r a l l e l m e m b r a n e s s e p a r a t e d b y a n a r r o w
b u t v a r i a b l e s p a c e o f l o w e l e c t r o n o p a c it y . T h e
n u c l e a r m e m b r a n e c a n b e se e n to b e p e r f o r a te d
a t f r e q u e n t i n t e r v a l s b y n u c l e a r p o r e s ( 5 1 ) . T h e
n u c l e a r m a t e r i a l i n w e l l f i x e d s p e c i m e n s i s e v e n l y
d i s t r i b u t e d , f i n e l y d i s p e r s e d , a n d g r a n u l a r . I n
i n a d e q u a t e l y f i xe d s p e c im e n s i t i s c l u m p e d w i t h
c l e a r a r e a s b e t w e e n t h e c l u m p s .
T h e n u c l e o l u s ( F i g . I 0 ) a p p e a r s a s a n a g g r e g a -
t i o n o f cl o s e l y p a c k e d , v e r y d e n s e g r a n u l e s o f
v a r i a b l e s i z e . A t o n e s i d e o f t h e n u c l e o l u s i s t h e
n u c l e o l a r b o d y w h i c h h a s a d i f f e r e n t p a t t e r n o f
g r a n u l a r i t y . I n p e r m a n g a n a t e - f i x e d m a t e r i a l , t h e
d e n s e g r a n u l a r m a t e r i a l i n t h e n u c l e o l us i s n o t
f i x e d a n d t h e r e r e m a i n s a f a i n t l y s t a i n e d b a c k -
g r o u n d a g a i n st w h i c h a n u m b e r o f fi n e d e n s e
f i l a m e n t s m a y b e s e e n , b u t t h e n u c l e o l a r b o d y i s
u n c h a n g e d i n a p p e a r a n c e .
FIGURE 5
Th i s mi c ro g r a p h sh o ws a se c o n d a ry d e n d r i t e o f a Pu rk i n j e c e l l a t a p o i n t o f b ra n c h i n g .
T h e d e n d r i t i c c a n a l i c u li c a n b e s e e n r u n n i n g a p a r a l l e l c o u r se f r o m l o w e r l e f t to u p p e r
r i g h t . A few e l e me n t s o f e n d o p l a sm i e re t i c u l u m a n d m i t o c h o n d r i a (m) c a n b e se e n a t
t h e p e r i p h e ry o f th e d e n d r i t e . C l o se l y a p p l i e d t o t h e d e n d r i t e , o n e i t h e r s i d e, c l i mb i n g
f i b e rs c a n b e se e n c f ) . Ne u ro p i l i s r e a d i l y d i s t i n g u i sh e d a t t h e l o we r r i g h t a n d u p p e r
left . X 18,000.
172 THE JOURN AL OF CE LL BIOLOGY VOLUME 18, 1963
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ROBZRT M HERNDON Fine Structure of Purkin~e dl 173
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D I S C U S S I O N
T h e m u l t i v e s i c u l a r b o d i e s a n d d e n s e g r a n u l e s
i l l u s t r a t e d i n t h i s p a p e r a r e s i m i l a r t o t h o s e
d e s c r i b e d i n t h e h y p o t h a l a m u s o f g o l d f i sh 3 4 ,
3 5 ) , m i c e 2 5 ) , a n d c h i c k e n s 8 ) . T h e p r e s e n c e o f
t r a n s i t i o n f o r m s f r o m t h e m u l t i v e s i c u l a r b o d y t o
t h e d e n s e g r a n u l e s h a s b e e n t h o r o u g h l y d e s c r i b e d
a n d i l l u s t r a t e d b y P a l a y 3 4 ) i n p r e o p t i c n e u r o n s
o f t h e g o l d f is h , a n d t h e s e s a m e t r a n s i t i o n f o r m s
a r e s e e n i n t h e r a t P u r k i n j e c e l l . E n z y m e s t u d i e s
c a r r i e d o n a t t h e e l e c t r o n m i c r o s c o p e l e v e l o n
s i m i l a r d e n s e g r a n u l e s i n c e l l s o f t h e s p i n a l c o r d
r e v e a l a c i d h y d r o l a s e a c t i v i t y i n t h e s e g r a n u l e s
2 8 ) a n d , a s a r e s u l t o f t h e s e s t ud i e s , N o v i k o f f
c o n s i d e r s t h e m t o b e l y s o s o m e s .
C h o u i n a r d 2 ) h a s d e s c r i b e d t w o t y p e s o f
g r a n u l e s s e e n i n t h e P u r k i n j e c e l l o f t h e c a t w i t h
l i g h t m i c r o s c o p y . T h e f i r s t t y p e h a s t h e h i s t o -
c h e m i c a l c h a r a c t e r is t i c s o f a n e u t r a l m u c o p o l y -
s a c c h a r i d e a n d i s d i f f u s e l y d i s t r i b u t e d t h r o u g h o u t
t h e b o d y o f t h e c e l l. T h e s e c o n d t y p e i s l i p o f u s c i n
a n d i s f o u n d m a i n l y i n c l u m p s a b o u t t h e b a s e o f
t h e d e n d r i t e a n d i n t h e m a j o r d e n d r i t i c b r a n c h e s .
T h e s i ze a n d d i s t r ib u t i o n o f t h e g r a n u le s i n o u r
m a t e r i a l s e e m t o c o r r e s p o n d w i t h t h o s e o f t y p e 1 ,
a n d l i p o f u s c i n h a s n o t b e e n s e e n i n o u r m a t e r i a l
p r e p a r e d f o r l ig h t m i c r o s c o py . T h i s i s p r o b a b l y
d u e t o t h e y o u n g a g e o f t h e a n i m a l s u s e d b o t h
f o r l i g h t a n d e l e c t r o n m i c r o s c o p i c s t u d i e s . T h e
e l u c i d a t i o n o f t h e t r u e n a t u r e o f t h es e g r a n u l e s
a n d t h e i r r e l a t i o n s h i p t o l y s o s o m e s , n e u t r a l m u c o -
p o l y s a c c h a r i d e g r a n u l e s , o r l i p o f u s ci n g r a n u l e s
a w a i t s f u r t h e r s t u d y .
M a l h o t r a a n d M e e k 2 4 ) i n t h e i r s t u d y o f t h e
P u r k i n j e c e l l s o f o w l s e x p r e s s e d t h e o p i n i o n t h a t
t h e r e i s t o o li t t l e a g r a n u l a r r e t i c u l u m i n t h e P u r -
k i n j e c e l l f o r i t t o b e t h e e q u i v a l e n t o f t h e G o l g i
a p p a r a t u s o f l i g h t m i c r o s c o p y . T h e i r v i e w , h o w -
e v e r , i s b a s e d o n i m m e r s i o n - f i x e d m a t e r i a l i n
w h i c h w e c o n s i d e r t h e g r a n u l a r e n d o p l a s m i c
r e t i c u l u m t o b e d i l a t e d a t t h e e x p e n s e o f o t h e r
i n t r a c e l l u l a r s p a c e s . I n i m m e r s i o n - f i x e d m a t e r i a l ,
m a n y o f t h e e le m e n t s o f a g r a n u l a r r e t i c u l u m a r e
n o t r e c o g n i z a b l e . F i g . 3 i s r a t h e r t y p i c a l o f th e
P u r k i n j e c e l l s e e n a f t e r p e r f u s i o n f i x a t i o n ; t h e
a g r a n u l a r r e t i c u l u m c o n f o r m s i n e x t e n t a n d
d i s t r i b u ti o n w i t h t h e G o l g i a p p a r a t u s o f li g h t
m i c r o s c o p y c o m p a r e F i g s. 2 a n d 3 ) .
T h e d i f f e re n c e in a p p e a r a n c e o f t h e n u c l e o lu s
i n p e r m a n g a n a t e - f i x e d m a t e r i a l i s d u e t o t h e
p e r m a n g a n a t e w h i c h d o e s n o t f i x t h e n u c l e o l a r
R N A a s do e s o s m i u m t e t r ox i d e . T h e r e m a i n i n g
d e n s e f i l a m e n t o u s m a t e r i a l i n t h e n u c l e o l u s a f t e r
p e r m a n g a n a t e f i x a ti o n m a y r e p r e s e n t t h e n u cl eo . -
l o n e m a 6 , 5 1 ) .
T h e i n t e r e st i n g a s s o c ia t io n o f m i t o c h o n d r i a a n d
s u b s u r f a c e c i s t e r n s s u g g es t s a n u m b e r o f p os s i b l e
f u n c ti o n s. A n a r r a n g e m e n t o f t h is s o r t m i g h t b e
v e tT u s e f u l i n s u p p l y i n g h i g h e n e r g y p h o s p h a t e s
s u c h a s A T P , p r o d u c e d b y th e m i t o c h o n d r i a , t o
a s t r u c t u r e w h i c h m i g h t b e i n v o l v e d i n t he a c t i v e
t r a n s p o r t o f m e t a b o l i t e s i n t o o r o u t o f t h e c e l l.
T h e c l os e a s s o c ia t io n a n d a p p a r e n t c o n t i n u i t y o f
t h e s e s t r u c tu r e s w i t h t h e g r a n u l a r e n d o p l a s m i c
r e t i c u l u m s u g g e s t s t h e p o s s i b i l i t y t h a t t h e s e
s t r u c tu r e s c o n t r o l t h e m o v e m e n t o f m a t e r i a l i n t o
a n d o u t o f t h e c h a n n e ls o f t h e e n d o p l a s m i c
r e t i c u l u m .
I n v e s t i g a t i o n s c a r r i e d o u t o n l i v i n g t is s u e c u l -
t u r e s h a v e s u g g e s t e d t o s o m e i n v e s t i g a t o r s t h a t
m i t o c h o n d r i a m i g r a t e f r o m t h e r e g i o n o f t h e
n u c l e u s t o t h e p e r i p h e r y a n d b a c k , a n d t h a t
m i t o c h o n d r i a m i g h t m a k e u s e of an a r r a n g e m e n t
s u c h a s t h e s u b s u r f a c e c i s t e r n to p i c k u p m e t a b o -
t~IGURE
Ne a r t h e c e n t e r o f t h i s mi c r o g ra p h i s a n a x o d e n d r i t i c sy n a p se c i rc le d ) . Th e t e rm i n a l
a x o n a l e n l a rg e m e n t , w h i c h i s a b o v e , c o n t a i n s n u me ro u s sy n a p t i c v e s ic l e s , a n d a
mi t o c h o n d r i o n i s r e a d i l y se e n . B e t we e n t h e p rc sy n a p t i c a n d p o s t sy n a p t i c me mb ra n e s ,
a t h i n d e n se l i n e a r ro w) c a n b e se en . At t h e l e f t i s a s e c o n d a ry b ra n c h o f a Pu rk i n j e
c e l l d e n d r i t e wh i c h c o n t a i n s a m i t o c h o n d r i o n a t m . Th e o r i g i n o f t h e d e n d r i t i c sp i n e
ma k i n g sy n a p t i c c o n t a c t i s o u t o f t h e p l a n e o f s e c t io n . X 4 2 ,0 0 0.
FIGURE
7
Th i s mi c r o g ra p h sh o ws a n a x o so m a t i c sy n a p se c i rc le d ) . Ne a r t h e c e n t e r o f t h e f i g u re
i s t h e e n l a rg e d sy n a p t i c t e rmi n a l p ro b a b l y o f a b a sk e t c el l ) c o n t a i n i n g t wo mi t o -
c h o n d r i a a n d n u me ro u s sy n a p t i c v e s i cl e s c l u s t e re d a b o u t t h e p re sy n a p t i c me mb ra n e .
To t h e l e f t i s t h e P u rk i n j e c e l l c y t o p l a sm. At t h e fa r l e f t , e l e me n t s o f t h e Go l g i a p p a ra t u s
G) are seen . M i toch ond rion , m; synapt ic vesic les, so. X 40 ,000 .
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lites at the periphery before migrating back to
the nuclear region 27). The absence of inter-
mediary forms may be considered to be evidence
against the interpretation that they are a stage in
the formation of mitochondria from the cell wall
44). It seems likely that these cisternae are in-
volved in the transport of some material into or
out of the Purkinje cell, but both the material
transported and the mechanism of transport
remain unclear.
At present, it is not possible to distinguish
excitatory from inhibitory synapses on a morpho-
logic basis. The evidence for the existence of two
functionally different synapses is well documented
physiologically 15) and it seems reasonable to
look for anatomical differences to correlate with
this. In the present study, we have confirmed the
R E F E R E N C E S
1.
BARGMANN W
and
KNOOP
A., Elektronen-
mikroskopische Beobachtungen an der Neuro-
hypophyse, Z . Z e l l f o r s c h . , 1957, 45, 242.
2. CHOUINARD, L. A., His tochemi cal cha rac ter -
istics of the PAS-positive inclusions in the
Purkinje cell of the cerebellar cortex in the
adult cat, C a n a d . J . Z o o l . , 1962, 40,87 1.
3.
DALTON
A. J., and FELIX, M. D., Studies on the
Golgi substance of the epithelial cells of the
epididymis and duodenum of the mouse,
A m . J . A n a t . , 1953, 92,277 .
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study of the Golgi complex, J . B i o p h y s i c . a n d
B i oc he m. Cy t o l . , 1956 2, No. 4, suppl., 79.
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mitochondria,
J . B i o p h y s . a n d B i oc h e m . C y t o l . ,
1956, 2, No. 4, suppl., 305.
6. DENUES, A. R . T., and MOTTRAM, F. C., Not e
on nucleolonemata in human cultured cells,
J . B i o p h y s i c . a n d B i o c h e m . C y t o l . , 1955, 1, 185.
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of the synapse,
In t e rna t . Re v . Cy t o l . ,
1960, 8,
61.
previous observations of Gray 18) who found that
cerebellar axosomatic and axodendritic synapses
differ in structure, the axodendritic synapse
demonstrating an additional dense line between
appositional surfaces of the cell membranes of
the synapse. It is tempting to speculate that the
presence of such a morphologic difference might
be correlated with a functional difference.
Dr. He rndon is a United States Public Health Service
postdoctoral Fellow at the Montreal Neurological
Institute.
The author wishes to express his thanks to
Dr. Huntington Sheldon and Dr. Gordon Mathieson
for their assistance and advice and to Miss Nora
Shepard who did most of the technical work.
R e c ei ve d f o r p u b l i c a t io n , N o v e m b e r 6 , 1 9 6 2 .
8. DUNCAN D., An electron microscope study of
neurohypophysis of
G a l l u s D o m e s t i c u s , A n a t .
Re c . , 1956, 125,457.
9. FERNXNDEZ-MORN, H., Ele ctr on microscopy
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in
Correlative Anat omy of the Nervous System,
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des ganglions spinaus 1),
A r c h . I t a l . B i o l . ,
1898, 30, 60.
FIGURE 8
In this micrograph of a Purkinje cell, four mitochondria can bc seen in close apposition
to subsurface cisterns arrows). A multivesi cular body ( m y ) and dense granules ( r )
can be readily distinguished. The nucleus and nuclear membrane can be seen at the
left X 10,500). Glycogen g) can be seen in a basket fiber at lower right.
I n s e t
at the
uppe r left is a higher power X 53,000) view of a mitoc hondri on in close appositi on
to a subsurface cistern. The arrow on the left indicates the mitochondrial membr anes.
The middle arrow points to the loop at the end of the subsurface cistern, and the a rrow
on the right indicates the cell surface membrane. Ju st above thc subsurface cistern an
indentati on in the cell membrane is seen, and just to the left of this, partially covered
by the arrows, is a ring s tructure , possibly a vesicle or cross-scction of a tubule.
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PALAY S. L.
T h e f i n e s t r u c t u r e o f s e c r e t o ry
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m ~ s a c e r c a d e l c r e c i m i e n t o y e v o l u c i 6 n d e s
FIGURE 9
I n t h i s m i c r o g r a p h o f P u r k i n j e c e ll cy t o p l a sm , t h e n u c l c a r m e m b r a n e c a n b e s e e n a t
t h e l o w e r l e f t . G r a n u l a r e n d o p l a s m i c r c t i c u l u m er), R N P g r a n u l e s , m i t o c h o n d r i a
( m ) a n d G o l g i a p p a r a t u s ( G ) a r e e as i l y s e e n . T h r e e d e n s e g r a n u l e s o f v a r y i n g d c n s i t y
a n d s i z e a r e a p p a r e n t ( g r ) . T h e l a r g e s t g r a n u l e c o n t a i n s a v a c u o l e ( v ) . W i t h i n t h e
v e s i cl e s o f t h e G o l g i a p p a r a t u s ( a r ro w s ) s o m c d e n s c g r a n u l a r m a t c r i a l c a n b e s e e n.
X 3 4 , 5 0 0 .
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Fin Structure of Purkinje ell
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FIGURE 1
This e le c t ron m ic rogra p h de m ons t r a te s the nucle o lus (n) a nd the nuc le o la r body ( a r row) . E le-
men ts of the Golgi ne twork , a dense body , and mito cho ndr ia are present a lso. X 13,000.
las f ibras cerebelosas ,
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