the fine structure of the purkinje cell

8/11/2019 The Fine Structure of the Purkinje Cell

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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

Published July 1, 1963


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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



5/14

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



6/14

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



7/14

ROBZRT M HERNDON Fine Structure of Purkin~e dl 173



8/14

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 .

174 T ~ JOURNAL OF CELL BIOLOGY VOLUME 18 1963



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ROBERT M HERNDON Fine Structure of Purldnje ell 175



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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 .

4. DALTON, A. J. , and FELIX, M. D. , A com par at ive

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.

5. DEMPSEY, E. W. , Varia tions in t he s truct ure of

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.

7. DE ROBERTIS, E., Submi croscopi c morphol ogy

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

of nervous tissue, Metabolism of the Nervous

System, New York, Pergamon Press, 1.

10. Fox , C. A., and BARNARD, J. W., A quant it ati ve

study of the Purkinje cell dendritic branchlets

and their relationship to afferent fibers, J.

A n a t . L o n d . , 1957, 91, 299.

11. Fox, C., The structure of the cerebellar cortex,

in

Correlative Anat omy of the Nervous System,

New York, Macmilla n Co., 1962, 193.

12. GOLGI, C., Sulla str uttu ra della sostanz a grigia

del cervello~ G a z z . m e d . i t a l . , 1873, No. 31,

244-246.

13. GOLGI, C., Unt ers uchu ngen fiber de n fei neren

Bau des centralen und peripherischen Nerven-

systems, Tr. by R. Teuscher), Jena , G.

Fischer, 1894.

14. GOLGI, C., Sur la struc ture des cellules nerveuses

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.

176 THE JOURNAL OF CELL BIOLOGY VOLUME 18, 1963



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ROBERT M HWRNDON Fine Structure of Purldnje ell | 77



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15. GRANIT R . , a n d PHILLIPS C. G. E x c i t a t o ry a n d

i n h i b i t o r y p r o c e s s e s a c t i n g u p o n i n d i v i d u a l

P u r k i n j e c e l l s o f t h e c e r e b e l l u m o f c a t s , J .

Phys io l . , 1 9 5 6 , 1 3 3 , 5 2 0 .

1 6. G R A Y , E . G . , A x o - s o m a t i c a n d a x o - d e n d r i t i c

s y n a p s e s o f t h e c e r e b r a l c o r t e x : a n e l e c t r o n

m i c r o s c o p e s t u d y , J . A n a t . , 1959 , 93 , 420 .

1 7. G R A Y , E . G . , E l e c t r o n m i c r o s c o p y o f d e n d r i t e s

a n d a x o n s o f t h e c e r e b r a l c o r t e x , J. Physiol. ,

1959 , 145 , 25P.

1 8. G R A Y , E . G . , T h e g r a n u l e c e ll s , m o s s y sy n a p s e s

a n d P u r k i n j e s p i n e s y n a p s e s o f t h e c e r e b e l l u m :

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 e o b s e r v a t i o n s ,

J . A n a t . ,

1961 , 95 , 345 .

1 9 . GR A Y, E . G . , a n d GUI L L E R Y, R . W . , T h e b a s i s

f o r s i l v e r s t a i n i n g o f s y n a p s e s o f t h e m a m -

m a l i a n s p i n a l c o r d : A l i g h t a n d e l e c t ro n

m i c r o s c o p e s t u d y , J. Physiol. , 1 9 6 1 1 5 7 , 5 8 1 .

20. HARTMANN J. FRANCIS E l e c t r o n m i c r o s c o p y o f

m i t o c h o n d r i a i n t h e c e n t r a l n e r v o u s s y s t e m ,

d . B iophys ic . and B iochem. Cyto l . ,

1956 , 2 , No . 4 ,

su p p l . , 3 7 3 .

21. ISSXDORIDES, M ., a nd SHANKLIN W. H i s t o -

c h e m i c a l r e a c t i o n s o f c e l l u l a r i n c l u s i o n s i n

t h e h u m a n n e u r o n e , J . A n a t . , 1961, 95, 151.

2 2 . L U F T , J . H . , I m p r o v e m e n t s i n e p o x y r e s i n e m -

b e d d i n g m e t h o d s ,

J . B iophys ic . and B iochem.

Cytol. , 1 9 6 1 , 9 , 4 0 9 .

2 3 . L U SE , S . A . , E l e c t r o n m i c r o s c o p i c o b s e r v a t i o n s

o f t h e c e n t r a l n e r v o u s s y s t e m ,

J . B iophys ic .

and Biochem. Cytol. , 1956 , 2 , 531 .

2 4 . M AL HOT R A, S . K . , a n d M E E K, G . A . , T h e e l e c -

t r o n m i c ro s c o p y o f t h e G o l g i a p p a r a t u s

o f t h e P u r k in j e c e l l s o f owl s ,

Q u a r t . J . M i c r .

So. , 1 9 6 0 , 1 0 1 , 3 8 9 .

D 5. M U R AK A M I, M . , E l e k t r o n e n m i k r o s k o p i s c h e U n -

t e r s u c h u n g d e r n e u r o s e k r e t o r i s c h e n Z e l l e n

i m H y p o t h a l a m u s d e r M a u s ,

Z. Zellforsch. ,

1962 , 56 , 277 .

2 6 . N I SS L , F . , U e b e r d i e s o g e n a n n t e n G r a n u l a d e r

N e r v e n z e l l e n , Neurol. Contr. , 1 8 9 4 , 1 3 , 6 7 6 .

2 7 . N OV l KO F F , A . B . , M i t o c h o n d r i a , in T h e C e l l ,

( J . B r a c h e t , a n d A . E . M i r s k y , e d i t o r s ) , 1 9 6 1 ,

N e w Y o r k , A c a d e m i c P r e s s , 2 , 2 9 9 .

2 8 . NOVlKOFF, A . B . , E SSNE R , E . , a n d HE u s , M . ,

E n z y m i c a c t i v i t i e s o f c y t o m e m b r a n e s ,

I n

Proe. 5 th In terna t . Congr . E lectron M icr . , N e w

Yo r k , Ac a d e m ic P r e ss , 1 9 6 2 , t . t . 2 .

29. PALADE G . E . , a n d CLAUDE A . , T h e n a t u r e o f

t h e G o l g i a p p a r a t u s . I . P a r a l l e l i s m b e t w e e n

t h e G o l g i a p p a r a t u s a n d i n t r a c e l l u la r m y e l i n

f ig u r e s ,

J . M o r p h o l . ,

1949 , 85 , 37 .

3 0 . P A L A D E, G . E . , E l e c t r o n m i c r o s c o p e o b s e r v a -

t i on s o f i n t e r n e u r o n a l a n d n e u r o m u s c u l a r

sy n a p se s ,

Anat . Reo . ,

1954 , 118 , 335 .

31 .

PALADE~ G. E.

A s m a l l p a r t i c u l a t e c o m p o n e n t

o f t h e c y t o p l a s m , J . B iophys ic . and B iochem.

Cyto l . ,

1955, 1, 59.

32. PALADE G. E.

a n d SE IKE VI TZ , P . , L iv e r m i -

c r o s om e s : A n i n t e g r a t e d m o r p h o l o g i c a l a n d

b i o c h e m i c a l s t u d y , J . B iophys ic . and B iochem.

Cyto l . ,

1956, 2, 171.

33. PALAY S. L. S y n a p s e s i n t h e c e n t r a l n e r v o u s

sy s t e m , J. Biophy sic. and Biochem. C ytol. , 1956,

2 , No. 4 , suppl . , 193 .

34.

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

n e u r o n s i n t h e p r e o p t i c n u c l e u s o f t h e g o l d -

f i s h ( C a r a s s i u s a u r a t u s ) , A n a t . R e c . , 1960,

1 3 8 , 4 1 7 .

3 5 . PAL AY~ S . L . , F i n e s t r u c tu r e o f n e u r o se c r e to r y

c e l l s i n t h e p r e o p t i c n u c l e u s o f f i sh e s , Proc.

European Reg iona l Con f . E lectron Micr . , De l f t ,

1 9 6 0 , 2 , 8 3 1 .

3 6 . PAL AY, S . L . , a n d PAL ADE , G . E . , T h e f i n e s t r u c -

t u r e o f n e u r o n s , J. B iophysic. and Biochem. Cytol. ,

1955 , 1 , 69 .

37 . PA LAY, S. L . , McGEE-RuSSELL, S. M . , GORDON,

S . , a n d GRILLO M. A. F i x a t i o n o f n e u r a l

t i s s u e f o r e l e c t r o n m i c r o s c o p y b y 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 , d . C e l l

B i o l . , 1962 , 12 , 385 .

3 8 . PE AC HE Y, L E E n . , A d e v i c e f o r s t a in in g t i s su e

s e c t i o n s f o r e l e c t r o n m i c r o s c o p y ,

J . B iophy~ ie .

and B iochem. Cyto l . , 1959 , 5 , 511 .

3 9 . P U R K IN J E, J . , V e r s a m m l u n g d e r N a t u r f o r s c h e r

u n d A e r t z e z u P r a g i m S e p t e m b e r 1 83 7,

I s i s yon Oken , 1 8 3 8 , 7 , 5 8 1 .

4 0 . R AM d N Y CAJAL S. E s t r u c t u r a d e l o s c e n t r o s

n e r v io so s d e l a s a y e s , in T r a b a j o s e s c o g i d o s

d e S . R a m 6 n y C a j a l, 1 8 8 0 -9 0 , M a d r i d , J u n t a

p a r a e l H o m e n a j e a C a j a l , 1 92 4, 1 , 3 0 5 - 3 1 5

( a p p e a r e d o r i g i n a l l y i n

Roy. Tr imes tra l H is to l .

normal y Pa to l . , M a y l , 1 8 8 8 ) .

4 1 . R AM d N Y CAJAL S. S o b r e c i e r t o s e l e m e n t o s

b i p o l a r e s d e l c e r e b e l o j o v e n y a l g u n o s d e t a l l e s

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 .

178 THE JOURNAL OF CEL L BIOLOGY VOLUME 18 1963



13/14

ROBERT M. HERNDON

Fin Structure of Purkinje ell

179



14/14

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 ,

op. cit.

517-535

(a ppe a re d or ig ina l ly in Gac. San. Barcelona

February 10, 1840) .

42. RAM6N Y CAJAL, S., Sur l or igin e e t la direc t i on

de s pro longa t ions ne rve use s de l a touc he

mol~cula ire du cervele t , op. cit. 4 5 1 - 4 8 5

(a ppe a re d or ig ina l ly in

Internat. Monatschr.

Anat. u. Physiol.

1889, 6, 158).

43. RAM6N v CAJAL, S., Histologie du systSme ner-

ve ux de l hom m e e t de s ve r tSbr6s , Ma dr id ,

Cons. Sup. Invest. Cient. Instituto Ram6n y Cajal

1952, 2, 1.

44. ROBERTSON, J . R. , Th e ul tra s truc ture of ce l l

m e m bra ne s a nd the i r de r iva t ive s ,

Biochem. Soc.

Symp. 1959, 16, 3.

45. ROSENBLUTH J. The f ine s t ruc ture of a c ous t i c

ga ngl ia in the r a t ,

J. Cell Biol.

1962, 12, 327.

46. ROSENBLUTH, J . , Subsurface c is terns a nd the i r

r e l at i o n s h ip t o t h e n e u r o n a l p l a s m a m e m b r a n e ,

J. Cell Biol. 1962, 13,405.

47. SItANKLIN, W. , ISSIDORIDES, M. , an d NASSAR,

T. K . , Ne urose c re t ion in the hum a n c e re -

be l lum ,

J. Comp. Neurol.

1957, 107, 315.

48. TALANTI, S. , and KIVALO E. , A ldehy de-fuch sin-

posi t ive granules in the P urkin je ce l ls of some

la bora tory a n im a ls , Ann. Med. Exp. et Biol.

Fenn.

1958, 36, 375.

49. THOMAS, O. L. , A co mpa ra t iv e s tud y of the

c yto logy of the ne rve c e l l w i th r e fe re nc e to

the proble m of ne urose c re t ion ,

J. Comp.

Neurol.

1951, 95, 73.

50. WATSON, M. L. , Sta in ing of t issue sec t ions for

e le c t ron m ic rosc opy wi th he a vy m e ta l s . I I .

Appl ic a t ion of so lu t ions c onta in ing l e a d a nd

b a r i u m ,

J. Biophysic. and Biochem. Cytol.

1958,

4, 727.

51.

WISCHNITZER S.

T h e u l t r a s tr u c t u r e o f t h e

nuc le us a nd nuc le oc ytopla sm ic r e la t ions , in

Internat. Rev. Cytol. 1960, 10, 137.

52. ZETTER~VIST H.

T h e u l t r a s t r u c t u r a l o r g a n i -

z a t ion of the c o lum na r a bsorp t ive c e l l s of

the m ouse j e junum , Ak t ie bola ge t Godvi l ,

Stockholm, 1956.

180 THE JOURNAL OF CE LL BIOLOGY VOLUME 18,

1963


the fine structure of the purkinje cell

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