bastian (1995) pyramidal-cell plasticity in weakly electric fish a mechanism for attenuating...

8/11/2019 Bastian (1995) Pyramidal-cell Plasticity in Weakly Electric Fish a Mechanism for Attenuating Responses to Reafferent Electrosensory Inputs

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J Com p Physiol A (1995) 176:63-78 9 Springer-Verlag 1995

J. Bast ian

P y r a m i d a l c e l l p l a s t i c it y i n w e a k l y e l e c t r i c f is h :

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

Accepted: 22 Jun e 1994

A b s t r a c t Record ings wi th in the pos te r io r eminen t ia

g ranu lar i s o f the weak ly e lec t r i c f i sh , Apterono tus l e -

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

un i t s respons ive to chan ges in the pos i t ion o f the an i-

ma l ' s t runk and tai l. In t race l lu la r l abe l l ing show ed tha t

t h e p ro p r i o c e p t o r r e c o rd i n g s w e re m a d e f ro m a x o n s t h a t

r a m i fy e x t e n s i v e ly w i t h i n t h e EG p . Th e l o c a t i o n o f th e

somata g iv ing r i se to these axons i s p resen t ly unknown.

Elec t ro recep to r a f fe ren t responses to e lec t r i c o rgan d i s -

c h a rg e a m p l i t u d e m o d u l a t i o n s c a u s e d b y m o v e m e n t o f

t h e a n i m a l ' s t a i l w e re c o m p a re d t o r e s p o n s e s c a u s e d b y

e l e c t ro n ic a l l y g e n e ra t e d A M s o f s i m i la r a m p l i tu d e a n d

t ime course . These d id no t d i f fe r . Elec t rosenso ry l a te ra l

l ine lobe py ramida l ce l l s responded s ign i f i can t ly l es s to

e lec t r i c o rgan d i scharge ampl i tude modu la t ions caused

b y c h a n g i n g t h e a n i m a l ' s p o s t u r e a s c o m p a re d t o e l e c -

t ron ica l ly p roduced AMs, sugges t ing tha t cen t ra l mecha-

n i sms a t t enua te py ramida l ce l l responses to reaf fe ren t

e lec t rosenso ry inpu ts . Exper imen ts in wh ich the pa t t e rn

of reaf fe ren t inpu t as soc ia ted wi th change s in pos tu re

was a l t e red revea led tha t the py ramida l ce l l s l earn , over a

t ime course o f severa l minu tes , to re jec t new pa t te rns o f

inpu t . Bo th p ropr iocep t ive inpu t and descend ing e lec t ro -

senso ry inpu t to the pos te r io r eminen t ia g ranu lar i s a re

invo lved in genera t ing the observ ed p las ti c change s in

pyramida l ce l l respons iveness .

K e y w o r d s P y r a m i d al c e ll s 9Neuronal p las t i c i ty

Lo n g - t e rm d e p re s s i o n 9 R e a f f e r e n t i n p u t

Weak ly e lec t r i c f i sh

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

A M a m p l i t u d e m o d u l a t io n

E G p pos te r io r eminen t ia g ranu lar i s

E L L e lec t rosenso ry l a te ra l l ine lobe

E O D e lec t r i c o rgan d i scharge

H R P h o r s e r a d is h p e ro x i d a s e

L T D l o n g - t e rm d e p re s s i o n 9 L T P long- te rm po ten t ia t ion

J

Bastian

Department of Zoology , University of O klahoma,

Norman, OK 73019, USA

ntroduction

Weakly e lec t r i c f i sh possess an ac t ive senso ry sys tem

c o m p o s e d o f a n e l e c t r i c o rg a n l o c a t e d i n t h e a n i m a l ' s

t runk and ta il , and e lec t ro recep to rs sca t t e red over the

su rface o f the body . Dis to r t ions o f the e lec t r i c o rgan d i s -

c h a rg e (EO D ) f i e ld r e s u lt f r o m t h e p r e s e n c e o f n e a rb y

ob jec t s d i f fe r ing in conduct iv i ty f rom the su r round ing

water o r f rom the d i scharges o f o ther e lec t r i c f i sh. These

d is to r t ions a re encoded by the e lec t ro recep to rs and sub-

sequen t ly ana lyzed by the cen t ra l nervous sys tem to ex -

t rac t behav io ra l ly re levan t in fo rmat ion . The moto r ac t iv i -

t i es o f weak ly e lec t r i c f i sh a re a l so expec ted to a l t e r the

EO D . Th e s e a n i m a ls c o m m o n l y b e n d t h e ir t r u n k a n d ta i l

adop t ing an a rc- l ike pos tu re du r ing exp lo ra to ry move-

m e n t s a n d b o t h EO D s i m u l a t i o n s t u d i e s (H e i l i g e n b e rg

1975 ; Hosh imiya e t a l . 1980) and empi r ica l f i e ld mea-

su remen ts (Assad e t a l . 1990) show tha t these pos tu ra l

changes p roduce s ign i f i can t changes in EOD ampl i tude .

Propr iocep t ive pa thways , par t i cu la r ly those p rov id ing

data abou t the pos i t ion o f the t a il and t runk , co u ld sup p ly

in fo rmat ion needed fo r the co rrec t in te rp re ta t ion o f se l f -

imposed o r reaf fe ren t pa t t e rns o f e lec t rosenso ry inpu t .

The e tec t rosenso ry l a te ra l l ine lobe (ELL) i s the p r i -

m a ry e l e c t ro s e n s o ry p ro c e s s i n g a r e a w i t h i n t h e b r a i n o f

weak ly e lec t r i c f i sh . In add i t ion to the e lec t ro recep to r a f -

fe ren t p ro jec t ion , the ELL rece ives e lec t rosenso ry inpu ts

descend ing f rom h igher cen ters (Maler e t a l . 1981 ; Sas

and Maler 1983 ; Bas t i an 1986a ,b ; Bas t i an and Bra t ton

1990 ; Bra t ton and Bas t i an 1990) and inpu ts f rom o ther

senso ry sys tems , poss ib ly inc lud ing p ropr iocep t ive in fo r -

mat ion as wel l as co ro l la ry d i scharges o f moto r com -

mands (Sas and Maler 1987) . A s impl i f i ed d iag ram sum-

mar iz ing the c i rcu i t ry o f the EL L and i t s connec t ions

wi th o ther e lec t rosenso ry p rocess ing reg ions o f the b ra in

i s shown in F ig 1 . The ELL i s a mul t i l aminar s t ruc tu re ;

the recep to r a f fe ren t s t e rmina te wi th in the mos t ven t ra l

l aminae , the deep f iber l ayer (DFL) , wh i le the descend-

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

u l t imate ly p ro jec t to the ELL's do rsa l (DML) and ven t ra l

(V M L) m o l e c u l a r l a y e r s . Th e p r i n c i p a l ELL e f f e r e n t


2/16

6

~ ~ To TS

I [ P r ~ 7 6

' ~ ' - - M P

~ l S t o t h r

T

L _ _ . ~

G

E x c i t a t o r y < 1

I n h i b i t o r y 9

D M L

V M L

,~Bp // ~~NBPPyrL

R e c e p t o r DFL

~ ( a f f e r e n t s T

F i g . 1 S u m m a r y o f e l e c t r o s e n s o r y l a t e r a l l i n e l o b e c i r c u i t r y . BP

B a s i l a r p y r a m i d a l c e l l ; Bp b i p o l a r c e l l ; DFL d e e p f i b e r l a y e r ;

DML d o r s a l m o l e c u l a r l a y e r ; EGp p o s t e r i o r e m i n e n t i a g r a n u l a r i s ;

G I t y p e 1 g r a n u l e n e u r o n ; G2 t y p e 2 g r a n u l e n e u r o n ; Gr g r a n u l e

ce l l ; Gr L g r a n u l e n e u r o n l a y e r ; M p m u l t i p o l a r c e l l ; NBP

n o n b a s i l a r p y r a m i d a l c e l l ; N P n . p r a e e m i n t i a l i s ; NVL n e u r o n o f

t h e v e n t r a l m o l e c u l a r l a y e r ;

Proprio.

p r o p r i o c e p t i v e ;

P yr L

p y r a m i d a l c e l l l a y e r ; St s te l la te ce l l ; V M L v e n t r a l m o l e c u l a r l a y e r

neurons rece ive recep to r a f fe ren t inpu t e i ther d i rec t ly

(bas i l a r py ramida l ce l l s , BP) o r ind i rec t ly v ia an inh ib i -

to ry in te rneuron (nonbas i l a r py ramida l ce l l s , NBP) . The

pyramida l ce l l s , as wel l as severa l ca tegor ies o f inh ib i to -

ry in te rneurons inc lud ing the type 2 g ranu le ce l l s (G2)

a n d n e u ro n s o f t he v e n t r a l m o l e c u l a r l a y e r (N V L ) , e x -

tend la rge ap ica l dendr i t es in to the superf ic ia l mo lecu lar

l a y e r s w h e re t h e y r e c e i v e d e s c e n d i n g e l e c t ro s e n s o ry a n d

o ther inpu ts men t ioned above . These var ious inpu ts to

the py ramida l ce l l ap ica l dendr i t es , and to dendr i t es o f

inh ib i to ry neurons , a re though t to con t ro l py ramida l ce l l

ga in and recep t ive f i e ld p roper t i es (Bas t i an 1993 ; Bas t -

i an and Bra t ton 1990 ; Bra t ton and Bas t i an 1990 ; Shum-

wa y and Maler 1989 ; Maler and Mugnain i 1993) .

The ELL pyramida l ce l l s p ro jec t to the n . p rae-

eminen t ia l i s (NP) and to the to rus semic i rcu la r i s (Maler

e t a l . 1982) . The NE which a l so rece ives an inpu t f rom

the to rus , p ro jec t s back to the ELL c los ing an e lec t rosen -

s o ry f e e d b a c k l o o p . A x o n s o f N P b i p o l a r a n d s t e l l a t e

ce l l s p ro jec t d i rec t ly to the ELL (dashed l ines ) fo rming

i t s ven t ra l mo lecu la r l ayer wh i le the axons o f the NP

mul t ipo lar , fu s i fo rm, and po lymorph ic ce l l s p ro jec t to

the pos te r io r emine n t ia g ranu lar i s (EG p) , a mass o f cere-

J . B a s t i a n : P y r a m i d a l - c e l l p l a s t ic i t y

bel la r g ranu le ce l l s over ly ing the ELL (Sas and Maler

1983) . The axons o f the EGp g ranu le ce l l s ( typ ica l para l -

l e l f ibers ) p ro jec t to the ELL fo rming the l a rger do rsa l

m o l e c u l a r l a y e r . Th e EG p m a y a l s o r e c e i v e p ro p r i o c e p -

t ive inpu ts and co ro l la ry d ischarges o f moto r com ma nds

(S a s a n d M a l e r 1 9 8 7) , h e n c e th e EG p t o ELL p ro j e c t io n

m a y b e i n v o l v e d i n c o m p e n s a t i n g fo r t h e e l e c t ro s e n s o ry

conse quenc es o f moto r ac t iv ity . Recen t s tud ies o f e lec t -

ro r e c e p t io n i n e l a s m o b ra n c h s a n d o f m e c h a n o re c e p t i o n

in t e leos t s revea led mechan isms fo r adap t ive ly f i l t e r ing

t h e e l e c t ro - a n d m e c h a n o s e n s o ry c o n s e q u e n c e s o f t h e

a n i m a l s o w n m o v e m e n t s (B o d z n i c k a n d M o n t g o m e ry

1994 ; Montgomery and Bodzn ick 1994a ,b ) .

Th is s tudy descr ibes the phys io log ica l and ana tomica l

charac te r i s t i cs o f p ropr iocep t ive neu rons tha t p ro jec t to

t h e EG p . A l s o , e l e c t ro r e c e p t o r r e s p o n s e s a n d r e s p o n s e s

o f ELL pyram ida l ce l l s to the e lec t rosenso ry s t imul i re -

su l t ing f rom changes in the an imal ' s pos tu re were com-

pared w i th responses to s imi la r pa t t e rns o f e lec t rosenso -

ry s t imul i genera ted wi thou t changes in the an imals ' pos -

tu re. T he re la t ive in sens i t iv i ty o f py ramida l ce l l s to e lec t -

rosenso ry s t imul i resu l t ing f rom changes in pos tu re ind i -

c a t e t h e p r e s e n c e o f m e c h a n i s m s t h at e n a b l e p y ra m i d a l

ce l l s to re jec t the e lec t rosenso ry inpu ts as soc ia ted wi th

body movements ( reaf fe ren t inpu ts ) . Las t ly , exper imen ts

are descr ibed which demons t ra te tha t py ramida l ce l l re -

sponses a re h igh ly p las t i c . The i r ab i l i ty to re jec t a g iven

pat te rn o f reaf fe ren t e lec t rosen so ry inpu t changes w i th

the recen t s t imula t ion h i s to ry o f the sys tem. The pyrami-

da l ce l l s can l earn to adap t ive ly fi l te r ( re jec t ) d i f fe ren t

pa t te rns o f e lec t rose nso ry inpu t i f these a re p resen ted re -

pe t i tive ly . The c harac te r i s t ics o f EL L pyram ida l -ce l l

p las t i c i ty a re s t r ik ing ly s imi la r to the p las t i c e f fec t s de-

s c r i b e d fo r o t h e r e l e c t ro s e n s o ry a n d t h e m e c h a n o re c e p -

t ive lateral l ine system s (Bell 1981, 1982, 1984, 1986,

1989; Bel l and Grant 1989, 1992; Bel l et al . 1992, 1993;

B o d z n i c k a n d M o n t g o m e ry 1 9 9 4 ; M o n t g o m e ry a n d

B o d z n i c k 1 9 9 4 a ,b ) . B o t h t h e d e s c e n d i n g e l e c t ro s e n s o ry

and p ropr iocep t ive inpu ts p rov ide in fo rmat ion su f f ic ien t

fo r py ramida l ce l l re jec t ion o f reaf fe ren t inpu ts and the

express ion o f py ramida l -ce l l p las t ic i ty .

Methods

T h e w e a k l y e l e c t r i c f i s h Apteronotus leptorhynchus a n d Eigen-

mannia

s p . w e r e u s e d i n t h i s s t u d y . S u r g ic a l p r o c e d u r e s a n d m e t h -

o d s u s e d f o r i n t r a c e l l u l a r l a b e l l i n g w i t h H R P h a v e b e e n p r e v i o u s l y

desc r ibed (Bas t ian and Cour t r igh t 1991 ; Bas t ian e t a l . 1993) .

P h y s i o l o g i c a l s t u d i es

A n i m a l s w e r e s u s p e n d e d i n a p le x i g la s t a n k 3 0 x 3 0 x 7 c m d e e p a n d

a r t i f i c ia l l y r e s p i r a t e d w i t h a c o n t i n u o u s f l o w o f a e r a t e d w a t e r. W a -

t e r t e m p e r a t u r e r a n g e d f r o m 2 5 to 2 7 ~ a n d c o n d u c t i v i t y w a s

m a i n t a i n e d a t a p p r o x i m a t e l y 1 0 k f 2 . cm .

I n t r a c e l l u l a r r e c o r d i n g s w e r e m a d e w i t h b o r o s i l i c a t e p i p e t te s

f i l l e d w i t h e i t h e r 3 M K C I o r w i t h 3 M p o t a s s i u m a c e t a t e ; t h e se

h a d r e s i s t a n c e s r a n g i n g f r o m 8 0 t o 1 5 0 M r 2 . F o r l a b e l l i n g e x p e r i -

m e n t s , b o r o s i l i c a t e g l a s s p i p e t te s w e r e f il l e d w i t h 1 0 H R P i n l

M K C 1 p l u s 0 . 0 1 M T r i s a d j u s t e d t o p H 7 . 4 . T h e H R P - f i l l e d e l ec -


3/16

J . Bas t i an : Pyramid a l -ce l l p las t i c i ty

r n o v e m e n l

E

T r u n k

restraints

E O D M

E

AM onvolo o

F i g . 2 D i a g r a m o f a p p a r a t u s u s e d t o a p p l y p r o p r i o c e p t iv e a n d

e lec t rosensory s t imul i , see Methods fo r de ta i l s

t rodes were beve led in a j e t - s t r eam con ta in ing 0 .05 gm gamma

alumina pa r t i c les un ti l re s i s tance fe l l to l e ss than 100 Ms Ext ra -

ce l lu la r r ecord ings were m ade wi th m eta l f i l l ed g lass p ipe t t e s de -

s c r i b e d b y F r a n k a n d B e c k e t ( 1 9 64 ) .

Ta i l and t runk d i sp lac emen ts s imi la r to those p roduced by f ree -

ly moving an im als were gene ra ted as shown in F ig . 2 . The an i -

mal ' s sku l l was g lued to an immobi le head-ho lder and the t runk

was suppor ted by two t runk res t ra in t s made f rom g lass cap i l l a ry

tub ing . The t ip o f the t a i l was a t t ached to a movab le a rm which

was l inked to the d r ive mechan ism of an x -y p lo t t e r . Movement o f

the a rm resu l ted in d i sp lacem ent o f the t a i l th rough an a rc as i l lus -

t ra ted by the curved a r row in F ig . 2 . The ampl i tude and pe r iod o f

the approx imate ly s inuso ida l pa t t e rn o f t a i l movement was de te r -

mined by the se t t ings o f the func t ion genera to r tha t p rov ided a s i -

nuso ida l s igna l to the p lo t t e r . The a rc th rough which the t a i l was

m o v e d w a s m e a s u r e d v i a a p r o t r a c t o r m o u n t e d o v e r t h e t a il - m o v e -

ment a rm. The cauda l t runk suppor t was typ ica l ly p laced abou t

midway a long the l eng th o f the body , d i rec t ly benea th the p ivo t

po in t o f the a rm, so tha t on ly the cauda l 50 o f the t runk pa r t i c i -

pa ted in the t a i l d i sp lacement .

The EOD ampl i tude modula t ions tha t r e su l t f rom ta i l d i sp lace -

ments were recorded v ia an e lec t rode p laced on the su r face o f the

sk in , nea r - to o r wi th in the recep t ive f i e ld o f the ce l l under s tudy ,

and a second implan ted in the dorsa l muscu la tu re . The smal l EOD

AMs tha t r e su l t f rom ta i l movements a re mos t eas i ly quan t i f i ed by

m e a s u r i n g t h e e n v e l o p e o f t h e E O D w a v e f o r m r e c o r d e d a c r o s s t he

sk in . Th is was p roduced by rec t i fy ing and low-pass f i l t e r ing the

EOD ( ' p rec i s ion abso lu te va lue c i rcu i t ' , c i rcu i t 2 .42d . 1968 Ph i l -

b r ick /Nexu s app l ica t ions manua l ) . E lec t rosen sory s t imul i des igned

t o m i m i c t h e E O D A M s t h a t r e s u l t f r o m t a i l d i s p la c e m e n t s w e r e

p r o d u c e d e l e c t r o n i c a l l y b y m u l t i p l y i n g t h e E O D w a v e f o r m r e c o r d -

ed v ia e lec t rodes a t the an imal ' s head and ta i l by a su i t ab le modu-

la t ion waveform (e .g . the s inuso ida l waveform app l ied to the p lo t -

t e r tha t d i sp laced the t a i l ) . The resu l t ing modula ted ve rs ion o f the

EOD was a t t enua ted and app l ied to the f i sh v ia e lec t rodes on e i -

the r s ide o f the an imal (F ig . 2 , E l and E2) . Th is t echn ique p ro -

duced e lec t ron ic mimics tha t evoked recep to r a f fe ren t r e sponses

s imi la r to the responses resu l t ing f rom ta i l -d i sp lacem ent AM s.

Only recep to r a f fe ren t s and ELL pyramida l ce l l s hav ing recep-

65

r ive f i e lds wi th in the ros t ra l 30 o f an an ima l ' s body were se lec t -

ed fo r s tudy . Ex t race l lu la r da ta were p rocessed on - l ine and d i s -

p layed as pe r iod h i s tograms o r r as te r d i sp lays tha t r e la te the ce l l ' s

ac t iv i ty to the t a i l moveme nt cyc le , o r to the AM cyc le o f e lec t ron-

ica l ly p roduced s t imul i . In t race l lu la r da ta were recorded on m ag-

ne t ic t ape (Hewle t t Packard mode l 3960 , 3 .75 ips , FM mode)

a long wi th synchron iza t ion pu l ses ind ica t ing the t iming o f t a i l

m o v e m e n t s o r e l e c t r o n i c a l ly p ro d u c e d A M s , a n d l a t e r p r o c e s s e d

as above . In a l l exper iments the EOD waveform measured a t the

recep t ive f i e ld o f the ce l l under s tudy was recorded fo r l a te r mea-

s u r e m e n t o f A M a m p l i t u d es .

The phase o f each ce l l ' s peak response to cyc l ic t a i l d i sp lace -

m e n t o r e l e c t r o n i c a l l y p r o d u c e d A M s w a s d e t e r m i n e d b y c a l c u l a t-

ing the d i rec t ion o f the mean vec to r fo r each pe r iod h i s togram

(Batsche le t 1981) . The phase o f the ce l l ' s min imum f i r ing f re -

quency was t aken to be 180 ~ away f rom tha t o f the response peak .

M a x i m u m a n d m i n i m u m s p i k e f r e q u e n c i e s w e r e c o m p u t e d f r o m

13 b ins cen te red on the t imes o r phases o f the peak and min imum

responses , r e spec t ive ly . Mea ns a re g iven _+1 standard e r ro r un less

ind ica ted o the rwise .

Results

P r o p r i o c e p t i v e i n p u t t o t h e E G p

S i n g l e u n i t s w e r e r e c o r d e d w i t h i n t h e p o s t e r i o r e m i n e n t -

i a g r a n u l a ri s w h i c h r e s p o n d e d i n a n o n a d a p t i n g m a n n e r

t o d i s p l a c e m e n t s o f t h e a n i m a l ' s t r u n k a n d t a i l . T h e s e

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

a v e r a g i n g 7 7_ +7 .2 s p i k e s / s , a n d w e r e n o t s e n s i t i v e t o in -

c r e a s e s o r d e c r e a s e s i n t he a m p l i t u d e o f t h e a n i m a l ' s o n -

g o i n g E O D . N o r w e r e t h e y re s p o n s i v e to l o w - f r e q u e n c y

e l e c t r o s e n s o r y s t i m u l i w h i c h a c t i v a te a m p u l l a r y e l e c t r o -

r e c e p t o r s . T h e s e p r o p r i o c e p t i v e u n i t s w e r e s u b d i v i d e d

i n to t h r e e r e s p o n s e t y p e s . T y p e I c e l l s i n c r e a s e d f i r i n g

r a te a s t h e t ai l w a s d i s p l a c e d t o w a r d t h e s i d e o f t h e b o d y

i p s i l a t e r a l t o th e E G p r e c o r d e d f r o m a n d f i r in g d e c r e a s e d

w i t h c o n t r a l a t e r a l d i s p l a c e m e n t s ( F i g . 3A ) . T y p e I I c e l l s

b e h a v e d o p p o s i t e l y , d e c r e a s i n g f i r i n g w i t h i p s i l a t e ra l ,

a n d i n c r e a s i n g f i r in g f r e q u e n c y w i t h c o n t r a l a t e r a l d i s -

p l a c e m e n t s ( F i g . 3 B ) . T h e m a j o r i t y o f p r o p r i o c e p t i v e

c e l l s e n c o u n t e r e d ( 9 2 ) f e l l i n t o th e s e t w o c a t e g o r i e s .

T y p e I I I c e l l s ( 8 ) p r o d u c e d m a x i m u m f i r in g r a t e s w h e n

t h e a n i m a l ' s t r u n k a n d t a il w e r e a p p r o x i m a t e l y s t r a i g h t

( F i g . 3 C ) ; t h e s e t y p i c a l l y g a v e s m a l l e r c h a n g e s i n a c t iv i -

t y f o r a g iv e n d e g r e e o f t a i l d i s p l a c e m e n t .

T h e t a i l p o s i t i o n s a t w h i c h t h e c e ll s r e s p o n d e d m a x -

i m a l l y , e x p r e s s e d a s t h e p e r c e n t o f th e t o t a l d i s p l a c e m e n t

( t y p i c a l l y a n a r c s u b t e n d i n g + 4 5 ~ a r e s u m m a r i z e d i n

F i g . 3 D . T h e t y p e I a n d I I c e l l s ' p e a k r e s p o n s e s o c c u r r e d

n e a r t h e l im i t s o f t h e i m p o s e d t a i l m o v e m e n t . I n d i v i d u a l

c e l l s w e r e r a r e l y f o u n d t h a t w e r e ' t u n e d ' t o i n t e r m e d i a t e

a m o u n t s o f d i s p la c e m e n t .

F i g u r e 4 A s u m m a r i z e s t h e r e s p o n s e s o f t w o t y p e I

c e l l s ( c i r c l e s a n d t r i a n g l e s ) a n d o n e t y p e I I c e l l ( s q u a r e s )

t o c o n t i n u o u s s i n u s o i d a l ta i l m o v e m e n t s o f v a r io u s a m -

p l i t u d e s . C l e a r c h a n g e s i n f i r in g w e r e s e e n w i t h d i s p l a c e -

m e n t s o f l e s s t h a n ___5 a n d t h e a v e r a g e s l o p e s o f th e

b e s t - f i t l i n e s t o t h e s e d a t a i n d i c a t e a g a i n o f a p p r o x i -

m a t e l y 4 s p i k e s / s p e r d e g r e e o f ta i l d i s p l a c e m e n t . S i n c e

t h e i n c r e a s i n g t a i l d i s p l a c e m e n t a m p l i t u d e s o f F i g . 4 A


4/16

66

F i g . 3 A - C P e r i od h i s t o gr a m s

o f p r o p r i o c e p t i v e u n i t a c t i v i ty

dur ing con t inuous 0 .1 Hz

s i n u s o id a l d i s p l a c e m e n t o f t h e

ta il ( av e rage o f 5 cyc le s ) . D

H i s t o g r a m o f p r o p r i o c e p t i v e

u n i t s p h a s e o f p e a k r e s p o n s e

e x p r e s s e d a s p e r c e n t a g e o f

m a x i m u m d i s p l a c em e n t

2 5 0

2OO

w

5 0

8 . 1 o o

5 0

E

Z

B

T o m A I

J . Bas t ian : Py ramida l -ce l l p la s t ic i ty

c

: o 1 T . . . .

- l O O j k -

/ }

5 0

, l i p

0

+ 4 5 0 - 4 5 0 + 4 5 + 4 5 0 - 4 5 0 + 4 5

ipsilateral conlralateraJ ips ilateral ipsilateral con tralateral ipsilateral

T a i l d i s p l a c e m e n t ( d e g . )

n

Type I cel ls

Type I I cells

Type III cells

O ,

+ 4 0

~ a a t e ~

0 -4O 0

c o n t r a l a ~

+ 4 O

ipsilaleral

l

U I I I I I I t / I ~ I I

I

9 5 7 5 5 5 3 5 1 5 0 - 1 5

i[o6ilateralbend

r I I I 1

- 3 5 - 5 5 - 7 5 - 9 5

contralaleralbend

P o s i t i o n o f p e a k r e s p o n s e ( d i s p l a c e m e n t )

. - 4 5 ~

g t . o . , , , ,

u . 0 _ + 1 0 + 2 0 - + 3 0 _ + 4 0 _ +5 0

T a l l d i s p l a c e m e n t ( d e g . )

F i g . 4 A P l o t s r e l a ti n g c h a n g e i n f i r in g f r e q u e n c y ( m a x i m u m m i n u s

m i n i m u m f i r i n g f r e q u e n c y w i t h i n t h e d i s p l a c e m e n t c y c l e ) t o t h e

a m p l i t u d e o f t h e t a il d i s p l a c e m e n t f o r t w o t y p e I c e l l s

c i rc l e s

and

t r i a n g l e s )

and one type I I ce l l

s q u a r e s ) .

T h e

o p e n c i r c l e

a t +10 ~

s h o w s c h a n g e i n f i r i n g f r e q u e n c y d e t e r m i n e d f r o m i n t e r v a l h i s t o -

g ram s o f the type I I ce l l ' s ac t iv i ty du r ing s ta t ic _+10~ d isp lacem en ts .

B P l o t s r e la t i n g c h a n g e i n f i r i n g f re q u e n c y o f t h e s a m e t y p e I a n d I

ce l l s to cons tan t ampl i tude ta i l d i sp lacemen ts ( ind ica ted to the le f t

o f each l ine ) p resen ted wi th d i f fe ren t ve loc i t ie s

w e r e p r o d u c e d w i t h a c o n s t a n t ( 0 .2 H z ) o s c i l l a t i o n f r e -

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

m o v e m e n t a m p l i t u d e. T h e e f f e c t o f v e l o c i t y a lo n e w a s

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

a r c a t v a r i o u s o s c i l l a t io n f r e q u e n c i e s . T h e e f f e c t o f v e -

0 10 20 30 40

T a i l v e l o c i t y ( d e g . / s )

l o c i t y i s s m a l l a s s h o w n b y F i g . 4 B ; t h e s e c e l l s i n c r e a s e

f i r in g r a t e b y a n a v e r a g e o f 0 . 8 s p i k e s / s p e r d e g r e e / s i n -

c r e a s e i n ta i l v e l o c i t y . T h e p r o p r i o c e p t i v e n e u r o n s a r e

a p p r o x i m a t e l y f i v e - f o l d m o r e s e n s i t i v e t o p o s i t i o n

c h a n g e s a s c o m p a r e d t o c h a n g e s i n v el o c i t y .

T h e s e p r o p r i o c e p t i v e u n i t s e n c o d e t a i l p o s i t i o n i n a

p r e d o m i n a n t l y n o n a d a p t i n g m a n n e r ; s t a t ic d i s p l a c e m e n t s

r e s u l t in o n l y s l i g h tl y s m a l l e r c h a n g e s i n f i ri n g f r e q u e n c y

a s c o m p a r e d t o w h e n t h e t ai l i s d y n a m i c a l l y d i s p l a c e d b y

t h e s a m e a m o u n t . T h e o p e n c i r c l e o f F i g . 4 A i n d i c a t e s

t h e d i f f e r e n c e i n f ir i n g f r e q u e n c y s e e n w i t h t h e t y p e I I

c e l l a s a r e s u l t o f c h a n g i n g t h e s t a t i c p o s i t i o n o f th e t a i l

f r o m + t o - 1 0 ~


5/16

J . B a s t i a n : P y r a m i d a l - c e l l p l a s t i c i ty

Fig. 5A Reconstructionof

HRP filled proprioceptive axon

recorded within he EGp. B Pe-

riod histogram of this cell's re-

sponses to 5 replicates of a 0.1

Hz _+45~ tail displacement

67

B

150]

IO0-

Q .

C 0 5 O

F r o m

L R N ? o -

45 0 . .45 0 45

i p s il a te r a J c o n t m l a t e r a l i p s il a te r a l

T a il d i s p l a c e m e n t d e g . )

Anatomy o f proprioceptive units

The identity of the EGp units giving proprioceptive re-

sponses was determined by recording intracellularly and

filling the cells with HRP or Lucifer yellow. In all cases

the fills showed that the type I and type II responses

were recorded from axonal plexi similar to that shown by

the reconstruction of Fig. 5A. An example of this recon-

structed type I cell's response to tail displacement is

summarized in Fig. 5B. The parent axons of these arbor-

izations course ventro-dorsally entering the EGp at its

rostro-medial pole. The axons then branched profusely,

ramifying throughout the majority of the rostro-caudal

extent of the EGp, a distance of about 960 gm in this

case. The morphology of these proprioceptive afferents

is quite similar to that of the previously described elect-

roreceptive axons projecting from the NP to the EGp

(Bastian and Bratton 1990). No fills were sufficiently

complete to identify the cell bodies associated with these

axons, however extracellular injections of HRP or wheat

germ agglutinin HRP into the EGp retrogradely label

cells in the lateral reticular nucleus (Sas and Maler 1987

and this study). These lateral reticular nucleus cells may

relay spinal proprioceptive information to the EGp, but

additional studies are needed to verify this prediction.

No fills of type III cells have been made thus far.

Electroreceptors respond similarly to EOD AMs caused

by tail displacement and to electronic mimics of these

Sinusoidal displacement of the fish's trunk and tail caus-

es amplitude modulations of the EOD, the magnitude of

which varies with the size of an individual's EOD, with

the site on the body surface at which the AM is mea-

sured, and with the amplitude of the tail displacement.

Modulation amplitude generally ranged between 50 and

150 gV peak-to-peak for displacements ranging between

_+20 to 50 ~ These modulations, rough ly 1 to 5 of the

normal EOD amplitude, are well above threshold for the

electroreceptors.

An example of the effects of EOD AMs due to tail

displacement on a receptor afferent's firing is shown in

the period histogram of Fig. 6A. The envelope of the

EOD modulation resulting from the tail displacement is

2 6 0 A Recemer a f t. 260 .C Receotor a f f

2 4 0 ~ 2 4 0

2 2 0 ~ 2 2 0 "

9 . Q.

0 9 2 0 0 09 2 0 0

1 8 04 5 0 - 4 5 0 4 5 1 80 ,~ -5 0 - 4 5 0 4 5

i p s i c o n t r a i p s i . i p s i . c o n t r a i p s i .

Ta i l d isp lacem ent

d e g . )

~ ; 5 0 B t a i l b e n d A M ~ ; 50 , D M i m ic A M

o - : . 5 o i , o - ' . 5 o i ,

4 5 0 - 4 5 0 4 5 4 5 0 - 4 5 0 4 5

i p s i . c o n t r a ip s i . i p s i . c o n t r a i p s i .

Ta i l d isp lacem ent

d e g . )

v . o 9

6

g o 9

~_ , ,,I 50K 9 , .

0 4 0 8 0 1 ) 0 5 0 7 0 9 0 l i 0

Freq . change sp /s ) EO D AM pV p -p )

Ta i l-bend AM Ta i l-bend AM

F i g . 6 A , C P e r i o d h i s t o g r a m s s u m m a r i z i n g a s i n g l e e l e c t r o r e c e p -

t o r a f f e r e n t ' s r e s p o n s e t o A M s d u e t o t a i l d i s p l a c e m e n t a n d t o t h e

m i m i c A M , r e s p e c t i v e l y ( 5 c y c l e s a t 0 . 2 H z ) . B E n v e l o p e o f t h e

E O D A M d u e t o t a il d i s p l a c e m e n t a n d D t h e e n v e l o p e o f t h e e le c -

t r o n i c m i m i c . E S c a t t e r p l o t r e l a t i n g e a c h r e c e p t o r a f f e r e n t ' s r e -

s p o n s e t o t h e m i m i c A M t o t h a t r e s u l t i n g f r o m t h e t a i l - b e n d . F

S c a t t e r p l o t s h o w i n g t h e a m p l i t u d e s o f t h e m i m i c A M s a n d t h e

t a i l - b e n d A M s u s e d t o s t i m u l a t e t h e r e c e p t o r a f f e r e n t s

shown in Fig. 6B. In this case the peak-to-peak EOD

modulation, measured across the skin near the receptor's

location, was 58 gV and this resulted in a change in fir-

ing frequency averaging 29 spikes/s. The response o f the

same receptor afferent to electronically generated AMs

of similar amplitude and time course (mimic AM) is

shown Fig. 6C and the envelope of the mimic AM is

shown in Fig. 6D. The mimic AM's amplitude was 64

gV p-p and this caused a change in receptor afferent fir-

ing averaging 28 spikes/s. Figure 6E compares the re-


6/16

68

s p o n s e s o f 1 3 r e c e p t o r a f f e r e n t s t o A M s r e s u l t i n g f r o m

t a i l d i s p l a c e m e n t a n d t o s i m i l a r l y s i z e d m i m i c A M s . T h e

r e s p o n s e o f e a c h a f f e r e n t t o t h e m i m i c A M i s p l o t t e d

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

d i s p l a c e m e n t . M o s t p o i n t s f a l l c l o s e t o t h e s o l i d d i a g o n a l

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

t o t h e s e t w o s t i m u l i . T h e a v e r a g e c h a n g e i n a f f e r e n t f ir -

i n g f r e q u e n c y e v o k e d b y t h e m i m i c A M s , 5 3 . 9 + 6 . 1

s p i k e s /s , w a s n o t s i g n i f i c a n t l y d i f f e r e n t f r o m t h e a v e r a g e

o f r e s p o n s e s t o t h e t a i l d i s p l a c e m e n t A M s , 5 4 .3 _+ 8. 3

s p i k e s /s ( P = 0 . 9 8 , t - te s t ). T h e a m p l i t u d e o f th e m i m i c

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

t u d e d u e t o t a i l d i s p l a c e m e n t i n F ig . 6 E T h e a v e r a g e

m i m i c a m p l i t u d e , 7 4 . 7 + 3 .8 B V , w a s n o t s i g n i f i c a n t l y d i f -

f e r e n t t h a n t h a t d u e t o t a i l d i s p l a c e m e n t w h i c h a v e r a g e d

70.5_+3.9 BV (P=0.45, t - test ) .

E L L p y r a m i d a l c e l ls r e s p o n d d i f fe r e n t l y t o E O D A M s

c a u s e d b y t a il d i s p l a c e m e n t a n d t o e l e c tr o n i c m i m i c s

o f t h e s e

S i x b a s i l a r p y r a m i d a l c e l l s ( E - c e l l s ) a n d t h r e e n o n b a s i l a r

p y r a m i d a l c e l l s ( I -c e l l s) w e r e s t u d i e d u s i n g b o t h t a i l - d is -

p l a c e m e n t A M s a n d e l e c tr o n ic m i m i c s o f t he s e a s s t im u -

l i . Typ i ca l l y , severa l d i f f e ren t o sc i l l a t i on f r equenci es ,

r a n g i n g f r o m 0 . 1 t o 0 . 4 H z w e r e u s e d f o r e a c h c e l l . T h e

p e r i o d h i s t o g r a m o f F ig . 7 A s u m m a r i z e s t h e r e s p o n s e s o f

a b a s i l a r p y r a m i d a l c e l l t o 5 0 c y c l e s o f a 0 . 1 H z t a i l d i s -

p l a c e m e n t . D e s p i te t h e f a c t t h a t t h e E O D A M m e a s u r e d

w i t h i n t h e c e l l s r e c e p t i v e f i e l d , F i g . 7 B , w a s w e l l a b o v e

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

f i r in g w a s n o t s i g n i f i c a n t l y m o d u l a t e d b y t h e s t i m u l u s .

T h e p e r i o d h i s t o g r a m i s n o t d i f f e r e n t f r o m t h a t e x p e c t e d

f o r a c e l l f i r i n g r a n d o m l y ( n o n s i g n i f i c a n t R a l e i g h s t a t i s -

t ic , B a t s c h e l e t 1 9 8 1) . T h e c e l l s f i r i n g w a s c l e a r l y m o d u -

l a t e d b y t h e m i m i c A M ( A M w i t h o u t t a i l d i s p l a c e m e n t )

a s i s s h o w n i n F i g . 7 C ( P < < 0 . 0 5 , R a l e i g h s t a ti s ti c ) . T h e

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

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

( 9 8 B V p - p ) w a s s l i g h t l y s m a l l e r t h a n t h a t o f t h e A M d u e

t o ta i l d i s p l a c e m e n t ( 1 0 3 ~ V p - p ).

T h e r e s p o n s e s o f th e p o p u l a t i o n o f c e l ls s t u d i e d a r e

s u m m a r i z e d i n F ig . 7 E w h e r e e a c h c e l l s r e s p o n s e s t o t h e

e l e c t r o n i c a l l y g e n e r a t e d A M s a r e p l o t t e d a g a i n s t r e -

s p o n s e s r e s u l t i n g f r o m t a i l m o v e m e n t . T h e p y r a m i d a l

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

A M s ; t h e p o i n t s c l u s t e r a b o v e t h e d i a g o n a l l in e t h a t i n d i-

c a t e s e q u i v a l e n t r e s p o n s e s . T h e a v e r a g e p y r a m i d a l c e l l

c h a n g e i n fi r in g f r e q u e n c y i n r e s p o n se t o th e m i m i c A M ,

9 .8_+1.1 sp ikes / s , i s s i gn i f i ca n t l y g rea t e r (P =0 .00 5 , t - t es t)

t h a n t h e c h a n g e o f 5 .9 _+ 0 .8 sp i k e s / s c a u s e d b y t a i l -m o v e -

m e n t A M s . T h e a m p l i t u d e s o f t h e m i m i c A M s a n d t h o s e

d u e t o t a i l m o v e m e n t a r e c o m p a r e d i n F i g . 7 F a n d i n a l l

c a s e s t h e m i m i c A M s w e r e s m a l l e r , a v e r a g i n g 5 9 . 9 + 2 . 9

c o m p a r e d t o 6 5 . 7 + 3 . 0 B V p - p f o r t h e ta i l - d i s p l a c e m e n t

A M s .

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

l a r l y t o t a i l - d i s p l a c e m e n t A M s a n d t o m i m i c s o f t h e s e ,

E-cel l

20 ta i l-bend AM

o

45 0 -45 0 45

ipsi contra ipsi.

J. Bas tian: Pyramida l-cell plasticity

_ C E-cel l

U 7 mimic AM t lno

- O I . , 9 I

4 5 0 4 5 0 4 5

ipsi. contra ipsi.

Tail Displaceme nt deg.)

~ ; 1 0 0 B ta il -b e n d A M ~g 1 0 0 D m im ic A M

4 5 0 - 4 5 0 4 5 4 5 0 - 4 5 0 4 5

ipsi. con tra ipsi. ipsi. contra ipsi.

Tail Displaceme nt deg.)

9 o

f o

0 10 20 30 0 40 80 120

Freq. chang e sp/s) EOD AM I~V p-p)

Tai l-bend AM Tai l-bend AM

Fig. 7A ,C P eriod histograms sum marizing a bas ilar pyramidal

cell s responses to AM s result ing from tail displacement and to

mimic A Ms , respectively (50 cycles at 0.1 Hz ). The fine l ines indi-

cate raw data and the heavy l ines indicate data smoothed by a four

bin m oving average filter. B,D E OD envelope s of the tail-displace-

ment and mimic AM s, respectively. E Scatterplot relating each py-

ramidal cell s responses to m imic AMs and to AM s due to tai l dis-

placement. F Sca tter plot show ing the am plitudes of the m imic

AMs and the tai l-bend AM s u sed to st imulate the pyram idal cells

t h e E L L p y r a m i d a l c e l l s a r e s i g n i f i c a n t l y l e s s r e s p o n s i v e

t o t h e A M s a s s o c i a t e d w i t h c h a n g e s i n p o s t u r e . I n m a n y

c a s e s p y r a m i d a l c e l l s s h o w v i r t u a l l y n o r e s p o n s e t o A M s

t h a t a r e c l e a r l y a b o v e t h r e s h o l d f o r t h e e l e c t r o r e c e p t o r

a f f e r e n t s a s l o n g a s t h e s e A M s a r e c o u p l e d t o m o v e -

m e n t s o f t h e t r u n k a n d t a il . S i n c e t h e s e p o s t u r e c h a n g e s

a l s o s t r o n g l y a c t i v a t e p r o p r i o c e p t i v e i n p u t s t o t h e E G p ,

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

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

s o r y c o n s e q u e n c e s o f th e a n i m a l s o w n m o v e m e n t s .

S y n a p t i c p l a s t i c i ty i s i n v o l v e d i n p y r a m i d a l c e l l

i n s e n s i t i v i t y t o th e e l e c t r o s e n s o r y c o n s e q u e n c e s

o f c h a n g e s i n p o s t u re

F r e e - s w i m m i n g a n i m a l s g e n e r a t e m o r e c o m p l e x a n d

v a r i a b l e p a tt e r n s o f b o d y m o v e m e n t s t h a n t h o s e u s e d in

t h e s e e x p e r i m e n t s , h e n c e t h e p y r a m i d a l c e l l s w i l l n o r -

m a l l y b e e x p o s e d t o a ra n g e o f E O D m o d u l a t i o n a m p l i -

t u d e s a n d w a v e f o r m s . T h e r e f o r e c o n s i d e r a b l e f l e x i b i l i t y

i s e x p e c t e d i n w h a t e v e r m e c h a n i s m s a r e r e s p o n s i b l e f o r

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

p a t t e r n s o f e l e c t r o s e n s o r y s t i m u l i . R e c e n t s t u d i e s o f s e n -


7/16

J. Bastian: Pyramidal-cell plasticity

S t i m u l u sP a t t e r n

A N o rm a l E O D A M d u e t o t a il b e n d

+20 ~ 1 0 0 1

+20 0 - 20 0 +20

B a s i l a r P y r a m i d a l C e l l R e s p o n s e s

Ta -bend AM

A 2 ~ o A , ,

~ _ . - a 5 .

~ t . t - ; ~ : t . ' ~ : r

: ; ~ ~

.~_ _~ --~; : : r I .A . .~ 10

. . . . . ~ 0

+20 0 -20 0 +20 +20 0 -20 0

69

+ 2 0

B 1 Tail b e n d A M P L U S a d d i ti o n a l l o c a l A M B 2 T a il -b e n d A M + l o c a l A M

-2O

L o c a l

A M

jt j: - ' - : . : ' - : ' ~ l s ~ ~ ~ + 2 o

- . ~ . . 9 , . = . q

. . - , - . . . . . . o , ~ .

. ~ - : ' : ~ ' r 0 - 20 0 +20

>:1. - . ~ / - : . - . - w . . ; - ~ . .

,,, ~

. - .. .:~ :~ : .~. ~ -

~ - 3 0 0 9 9 . : % . . ~ . ~ ~ . I ~

+20 0 - 2 0 0 + 2 0 . . . - . - : . ~ t ~ . : ,

I -

+ + o ~ - ~ o 6 + o + 2 o o . 2 0 o + ~ o

Ct

N o rm a l E O D A M d u e t o t af t b e n d

C2

Ta i l -bend AM

: ~ 1 B ~ r : l

t a

, v . 4 # ' ~ . "

9 ~ a ~ o _ _ - ~ f ~ , , g ~ .~ a k ~ = ~ - . - - ' : . ; -, "

L ~ > I ~o 8 ~ ~ ~ . - . : _ ~ r

~.-~ .~ . .~ .~:~t . ~ . - . . .-_ . - . l

T a i l d i s p l a c e m e n t d e g . ) ~ : . . ~ . ~ , ~ . > ~ . - . ,, L = . ~ . . . : . ~ ; . ~

a 9 # l .e '~ '% ~ - - " " -

~ o ~ ~ o ~ ~ o 2 o o 2 0 o 2 0

T a i l d i sp l acem en t d eg . ) T a i l d i sp l acem en t d eg . )

F i g .

8A1 Diagram illustrating the tail displacement stimulus and

p y r a m i d a l c e l l s r e c e p t i v e f i el d , r e s u l t i n g f r o m + 2 0 ~ t a il

the measurement of the EOD waveform along with a plot of enve- di sp lac em en t (45 ~V p-p ), is sh ow n in F ig. 8A 1 and a

lope of EOD AM. A2 raster display of a basilar pyramidal cell 's

response to 20 cycles of a +20 ~ 0.4 Hz continuous sinusoidal ta il ras ter dis pla y of th e c el l ' s act ivi t y d ur ing ta i l m ov em en t

displacement. A3 Period histogram of the data shown in A2. B1 is sho w n in F ig . 8A2. F igu re 8A 3 is a per iod hi s to gr am

Diagram of the ta il displacement s t imulus plus the local s t imulus su m m ar izi ng this ras ter data . As de scr ib ed ab ov e, the

arrow)

a long wi th a p lot o f the EOD AM envelope resu lt ing f rom bas i l a r py ram ida l ce l l ' s ac t iv i ty i s no t m o du la te d by th i s

the combined st imuli. B2 Raster display of the cell 's response to s t im ulu s . A fte r com pl et i on o f these f i r s t 20 ta i l dis pla ce-

80 cycles o f the 0.4 Hz tail displacem ent plus the 0 .4 Hz local

EOD AM . B3,B4 Period histograms of data from the first and last m en t

c y c l e s , a n a d d i t i o n a l e l e c t r o n i c a l l y p r o d u c e d s i n u -

20 s tim ulus cycles o f B2 . C1 Diagram of the t ai l-bend s tim ulus so ida l AM , syn ch ron ize d to the t a i l -m ov em en t cyc le ,

and plot of the envelope of the resul ting EOD AM. C2 Raster dis- wa s lo cal ly ap pl i ed to th e f ish a t the s i te o f the py ra m id al

play of responses to 80 cycles of the ta il -bend s timulus alone, ce l l ' s re ce pt i ve f ie ld (ar row in the dia gr am of F ig. 8B 1).

C3,C 4 period histograms of responses to the first and last 20 stim-

u lu s c yc le s o f C 2 T h i s a d d i t i o n a l A M i n c r e a s e d t h e a m p l i t u d e o f t h e s t i m -

u l u s m e a s u r e d w i t h i n t h e c e l l 's r e c e p t i v e f i e l d t o a p p r o x -

i m a t e l y 3 0 0 g V p - p ( F i g . 8 B 1 ) . T h e c e l l i n i t i a l l y r e -

s o r y p r o c e s s i n g i n r e la t e d s y s t e m s ( B e l l 1 9 8 1 , 1 9 8 2 , s p o n d e d s t r o n g l y t o t h is n e w p a tt e r n o f e l e c t r o s e n s o r y

1 9 8 4 , 1 9 8 6 , 1 9 8 9 ; B e l l a n d G r a n t 1 9 8 9 , 1 9 9 2 ; B e l l e t a l. i n p u t , b u t t h e r e s p o n s e g r e w w e a k e r w i t h c o n t i n u o u s p r e -

1 9 9 2 , 1 9 9 3 ; B o d z n i c k a n d M o n t g o m e r y 1 9 9 4; M o n t - s e n t a ti o n o f t h e t a i l- b e n d p l u s t h e l o c a l A M ( F ig . 8 B 2 ) .

g o m e r y a n d B o d z n i c k 1 9 9 4 a , b ) h a v e s h o w n t h a t n e u - T h e r e s p o n s e d e c a y e d t o l e ss t h a n 5 0 % o f i ts i n it ia l v a l u e

t o n s , a n a l o g o u s t o t h e p y r a m i d a l ce l ls st u d i e d h e r e , h a v e o v e r t h e t i m e ( 2 0 0 s ) o f t h e 8 0 p a i r e d p r e s e n t a t i o n s o f

p l a s t i c p r o p e r t i e s t h a t a l l o w t h e m to a d a p t i v e l y f i l t e r s e n - t h e t a i l - b e n d p l u s l o c a l A M s t i m u l i . T h e p e r i o d h i s t o -

s o r y in p u t s r e s u l ti n g f r o m t h e a n i m a l ' s o w n a c t iv i ty . T o g r a m s o f F ig . 8 B 3 , B 4 s u m m a r i z e t h e d a ta f r o m t h e fi r st

t e s t t h e i d e a t h a t E L L p y r a m i d a l c e ll s c a n l e a r n o r a n d la s t 2 0 p r e s e n t a t i o n s , r e s p e c t i v e l y , o f t h e s e p a i r e d

a d a p t i v e l y r e j e c t v a r i e d p a t t e r n s o f e l e c t r o s e n s o r y i n p u t , s t i m u l i .

e x p e r i m e n t s w e r e d o n e in w h i c h a c e l l 's r e s p o n s e s w e r e F o l l o w i n g t h e 8 0 p r e s e n t a t i o n s o f t h e p a i r e d st i m u li ,

m o n i t o r e d w h i l e a l t er i n g t h e p a t t e r n o f e l e c t r o s e n s o r y i n - t h e l o ca l A M w a s r e m o v e d r e s t o r i n g t h e e l e c t r o s e n s o r y

p u t r e l a t e d t o t a i l m o v e m e n t , i n p u t d u e t o t a i l d i s p l a c e m e n t t o i t s o r i g i n a l p a t t e r n ( F i g .

T h e e n v e l o p e o f th e A M m e a s u r e d w i t h i n a b a s i l a r 8 C 1 ) . A l t h o u g h a t t h e st a rt o f t h e e x p e r i m e n t t h e c e l l


8/16

70

was unrespons ive to th is s t imu lus (F ig . 8A2 ,A 3) , i t re -

s p o n d e d v i g o ro u s l y t o t h e ta i l -b e n d A M a l o n e fo l l o w i n g

the per iod o f pa i red s t imula t ion (F ig . 8C2 ,C3) . T he phas -

es o f the exc i ta to ry and inh ib i to ry p o r t ions o f the re -

s p o n s e w e re , h o w e v e r , o p p o s i t e t h o s e s e e n w h e n t h e l o -

c a l A M w a s p a i r e d w i t h t h e t a i l d i s p l a c e m e n t ( c o m p a re

Fig . 8B3 ,C3) . The f i r ing pa t t e rn seen a f te r the pa i red

s t imula t ion i s very su rp r i s ing s ince bas i l a r py ramida l

ce l l s no rmal ly on ly increase f i r ing f requency in response

to

incre sing

EO D a m p l i t u d e . Th e n e w l y a c q u i r e d r e -

sponse to the t a i l -bend AM shows s t rong ly increased py-

ramida l ce l l ac t iv i ty apparen t ly in response to decre sing

EO D a m p l i tu d e . Th i s r e s p o n s e a l s o d e c a y e d w i t h c o n t in -

ued s t imulus p resen ta t ion (compare the per iod h i s to -

g rams o f F ig . 8C3 ,C4) .

Th is py ramida l ce l l response p las t i c i ty i s s imi la r to

t h a t d e s c r i b e d fo r ELL n e u ro n s o f m o rm y r i d e l e c tr i c f i sh

(Bel l 1981 , 1982) , fo r ce l l s wi th in the e lec t rose nso ry

sys tem o f e lasmobranc hs and w i th in the no rmal l a te ra l

l in e s y s t e m o f t e le o s t s (B o d z n i c k a n d M o n t g o m e ry

1994 ; Montgomery and Bodzn ick 1994a ,b ) . In a l l cases

the neurons invo lved a re ab le to re jec t pa t t e rns o f senso -

ry inpu t re la ted to the an imal ' s o wn a c t iv i ty pa t t e rns . T he

m e c h a n i s m b y w h i c h t h i s i s a c c o m p l i s h e d i n v o l v e s t h e

cen t ra l genera t ion o f wha t has been descr ibe d as a neg -

a t ive imag e o f the expec ted reaf fe ren t inpu t (Bel l 1984)

o r a c a n c e l l a ti o n s i g n al (M o n t g o m e ry a n d B o d z n i c k

1994b) . The increa sed respons iven ess o f the py ramida l

ce l l o f F ig . 8 to the t a il d i sp lacem en t a lone , seen a f te r the

loca l s t imu lus was pa i red fo r a t ime then removed , i s an

exam ple o f th i s nega t ive image response . The deve lop-

men t o f th i s nega t ive image inpu t to the py ramida l ce l l i s

respons ib le fo r the p rogress ive a t t enua t ion o f the ce l l ' s

response to the pa i red s t imul i show n in F ig . 8B2 .

Co inc idence o f t a i l -bend and loca l s timu l i a re necessary

The a t t enua t ion o f py ramida l ce l l responses to the loca l ly

app l ied AM on ly occurs i f th i s s t imu lus i s app l ied s imul -

taneous ly and in synchrony wi th the t a i l d i sp lacemen t as

show n in F ig . 9 . Again , th i s ce l l was in i t i a l ly u n respon-

s i ve t o th e A M d u e t o t ai l b e nd i n g ; t h e EO D A M d u e t o

ta i l bend ing , a ras te r d i sp lay o f the ce l l ' s respo nses and a

per iod h i s tog ram o f these da ta a re show n in F ig .

9 A 1 -A 3 . Th e l o c a l A M u s e d i n t h i s e x p e r i m e n t w a s i n

an t iphase re la t ive to tha t p roduced by the t a i l d i sp lace-

men t (F ig . 9A4 ) and the ba s i l a r py ramida l ce l l in it i a lly

respond ed s t rong ly to the r i s ing phase o f the loca l s t imu-

lus pa i red wi th the t a i l -bend s t imulus (F ig . 9A2 ,A5) . The

response d imin i shed wi th repe t i t ive p resen ta t ions as

show n by the ras te r and per iod h i s tog ram s o f da ta t aken

dur ing the f i r s t and las t 20 cyc les o f the pa i red s t imula-

t io n ( c o m p a re F i g . 9 A 5 ,A 6 ) . F o l l o w i n g t h e r e m o v a l o f

the loca l AM the ce l l responded s t rong ly to the t a i l -bend

A M a lone , and th is response w as a nega t ive image o f the

response to the p rev ious ly app l ied pa i red s t imul i (F ig .

9A8) .

When the ce l l was s t imula ted wi th the loca l AM in

J. Bastian: Pyram idal-cell plasticity

the absence o f s imul taneous t a i l d i sp lacemen t , ne i ther a t -

t enua t ion o f the response to the loca l AM, nor the deve l -

o p m e n t O f a n e g a t iv e i m a g e r e s p o n s e w a s s e e n . F o l l o w -

ing the in i ti a l p resen ta t ion o f the t a il d i sp lacem en t s t imu-

lus (F ig . 9B1-B3) , t a i l mo t ion was s topped and the loca l

A M w a s p r e s e n t e d a l o n e (F i g . 9 B 4 ) . Th e c e l l r e s p o n d e d

wi th a somewhat d i f fe ren t f i r ing pa t t e rn to the loca l AM

alone and responses remained cons tan t th roughou t th i s

per iod o f s t imula t ion (F ig . 9B5 ,B6) . Fo l lowing the ces -

sa t ion o f s t imula t ion wi th the loca l AM, ta i l d i sp lace-

men t was res to red , bu t the ce l l remained unrespons ive to

th i s s t imulus (F ig . 9B7 ,B8) . S ign i f i can t a t t enua t ion o f

pyramida l ce l l responses to the loca l AM and the appear-

a n c e o f n e g a t iv e i m a g e s o f e x p e c t e d i n p u t s o n l y o c c u r r e d

w h e n t h e l o c a l A M w a s p r e s e n t e d i n s y n c h ro n y w i t h t ai l

d i sp lacemen t .

P ro p r i o c e p t iv e a n d e l e c t ro s e n s o ry i n fo rm a t io n

can independen t ly med ia te p las t i c changes in py ramida l

ce l l respons iveness

The inpu ts to the py ramida l ce l l s g iv ing r i se to the nega-

t ive images o f expec ted inpu ts a re l ike ly to be rece ived

v ia the ce l l ' s ap ica l dendr i t es . As descr ibed above , p ro -

p r iocep t ive inpu ts a re p resen t wi th in the EGp, and th i s

in fo rmat ion wi l l be t ransmi t ted to the py ramida l ce l l ap i -

ca l dendr i t es v ia the ELL dorsa l molecu lar l ayer para l l e l

f ibers . The pyramida l ce l l s a l so rece ive in fo rmat ion

a b o u t a m p l i tu d e m o d u l a t i o n s o f t h e EO D f i e l d v ia D M L

para l l e l f ibers s ince the EGp rece ives nonadap t ing e lec t -

ro recep t ive inpu ts tha t descend f rom the nuc leus

p raeeminen t ia l i s (Bas t i an and Bra t ton 1991) . Add i t iona l -

ly , axons o f the NP s te l l a te and b ipo lar ce l l s p ro jec t d i -

rec t ly to the ELL ven t ra l mo lecu lar l ayer p rov id ing an -

o t h e r s o u rc e o f d e s c e n d i n g e l e c t ro s e n s o ry i n fo rm a t i o n t o

the ELL Pyramida l ce l l s (Sas and Maler 1983 ; Bra t ton

and Bas t i an 1990 ; Maler and Mugnain i 1994) . There-

fo re , d i sp lac ing the t a i l s imul taneous ly p rov ides bo th

propr iocep t ive and e lec t ro recep t ive inpu ts to the ELL py-

ramida l ce l l s ' ap ica l dendr i t es a long wi th the ascend ing

e lec t ro rec ep to r a f fe ren t inpu t .

Ex p e r i m e n t s w e re d o n e i n w h i c h l o c a l i z e d e l e c t ro se n -

s o ry s t i m u l i w e re p a i r e d w i t h w h o l e -b o d y p a t t e rn s o f

e l e c t ro s e n s o ry i n p u t w h i c h m i m i c t h e A M s g e n e ra t e d b y

ta i l d i sp lacemen t . S ince these mimic AMs were genera t -

ed in the absenc e o f ta i l d i sp lacem en t , th i s exper im en t

can de te rmine i f p ropr iocep t ive inpu t i s necess ry fo r

pyramida l -ce l l p las t i c i ty . Likewise , in o rder to de te rmine

i f w h o l e -b o d y e l e c t ro s e n s o ry s t i m u l i a r e n e c e s s a ry fo r

p las t i c i ty , exper imen ts were done in wh ich loca l e lec t ro -

senso ry s t imul i were pa i red wi th t a i l d i sp lacemen ts in

an imals whose e lec t r i c o rgan d i scharge was abo l i shed

(p ro p r i o c e p ti v e i n p u t w i t h o u t t h e a s s o c i a t e d w h o l e -b o d y

E O D A M ) .

Figure 10 summarizes an exper imen t in wh ich a loca l

0 .4 H z A M w a s p a i r e d w i t h a w e a k e r t a i l - b e n d m i m i c

A M o f t h e s a m e f r e q u e n c y a p p l i e d t r a n s v e r s e l y t o t h e

w h o l e a n i m a l v i a e l e c t ro d e s E l ,E 2 o f F ig . 2 . B o t h s ti m u -


9/16


Fig. 9A1, A4, A7 EOD AM

envelopes result ing from tai l

displacement (A1,A7) and tail

displacement plus a locally ap-

plied AM (A4). A2 Raster dis-

play o f a basilar pyramidal

cell 's responses to 20 cycles of

+_20~ 0.4 H z tai l displacement

followed by 100 cycles of the

paired local AM plus tail-bend

stimulus followed by 40 cycles

of the tail-bend stimulus alone.

A3, A5, A6 , A8 Period histo-

gram s of the data indicated by

the

l a b e l e d b r a c k e t s

to the right

of the raster display. B1, B 4,

B7 EOD AM envelopes due to

tail-bend stimuli (B1, B7) and

due to the local stimulus pre-

sented alone (B4). B2 Raster

display o f the ce ll 's responses

to 20 cycles of ___20~ 0.4 Hz tail

displacement followed by 100

cycles of the local AM alone

followed by 40 cycles o f the

tail-bend stimulus alone. B3,

B5, B6, B8 Period h istograms

of the data indicated by the

l a -

b e l e d b r a c k e t s

to the right of

the raster display

7 1

A 1

T - b e n d A M

A 2 A 3

1 5 0 ~ . . . . " " ~ - '

9 9 : . . . , ~ ' .. , .~ " . . - - - - . . - ~ , *

- - . ~ ,~

,, ~ ., '...; (. ,..

1

3

0 : . ' : r "

' - . . . : : . ' ' : ' l

~ ~ .

I ' t > ' - ~ ~ .r , ~ . " t t A 1

r - o " ; ' 1 ~

I , . M " - ' - - . ' . " " " "

~-~.. .~

' ~ ~

2 0 0 - 2 0 0 2 0

1 50 1A T r-...-~ ~ - - - - - T ' b e n dM : : : :

. /

1 , , . .

5 0

- . .

2 0 o - 2 o o 2 0 ~ , o 6 - ~ o 6 ; 0 2 0 0 - 2 0 0 2 0

T a i l D i s p l a c e m e n t ( d e g r e e s )

B 1 T - b e n d A M . . B 2 . . ,

1 5 0

. - r - . ~ . . L

o ~ . - r : , 4 .

. , - . , ~

- . ~.- .~ ~.

1 5 0 . , ' - ' . ' ~ , ,

+ 2 0 0 - 2 0 0 + 2 0 . . ,. ~ .

O . ~ ^ ^ B 4 L o c a l A M a l o n e

_ . : . . j = ,

> t

~ , - 3 0 0 F , , , - -

....,.:~ ~

,

+ 2 0 0 - 2 0 0 + 2 0

L U , ' I T S _ .

A - - o " ~ 9 m

. ' . . . . z

1 5 0 B T-bend AM 9 9 : .. ,

9 ~ ~ " ,

0 ~ . . o

9 ~ . c ~

-150

+ 2 0 0 - 2 0 0 + 2 0 + 2 0 0

9 . . - , - . - . . . = . , . .

r W k : . , ' . = -

~ , o " ~ 9 o ~ 9

~ r ; . ' . . . .

k . ; A " " . . "

~ . ' ~ , .' . - . 4 t

. .

: _ ~ . . . . . , L

' # ~ . 4 o " .

9 9 . . . .

S I ~ ~ ~ ~ L ~

~ . ~ . . . : . . - . ,

. ~ . . ~ : . '. ., .

: . - ~ - ; " , r ' , - - - " 9 /

; . - ' ~ k~ : ' , ', ~ ; ,

' * ~ -~ : T ' :. . : ; : ' B

: ' ." ' " " " " " " ' ; " 8

, t ; . , " . . ~ ' j " , . . , -

' , . e ' e r 9 ~ ' . ' . : ' 1 .

~ . . . . . ; : ,- . , .. ' + . .; , .: ' .

- 2 0 0 + 2 0

T a i l D i s p l a c e m e n t ( d e g r e e s )

+ 2 0

3 0 R R

1 5

0

+ 2 0

9 , , R R

+ 2 0

0 - 2 0 0 + 2 0

0 - 2 0 0 + 2 0

0 - 2 0 0 + 2 0

+ 2 0 0 - 2 0 0 + 2 0

l i w e r e g e n e r a t e d e l e c t r o n i c a l l y a n d t h e a n i m a l ' s p o s t u r e

r e m a i n e d u n c h a n g e d . T h i s b a s i l a r p y r a m i d a l c e l l r e -

s p o n d e d w e a k l y t o t h e w h o l e - b o d y A M p r e s e n t e d a l o n e

a s s h o w n b y t h e i n i t ia l p o r t i o n o f t h e r a s t e r d i s p l a y ( F i g .

1 0 A ) a n d t h e p e r i o d h i s t o g r a m o f t h e s e d a t a ( F i g . 1 0 B 1 ).

T h e m a g n i t u d e o f th e w h o l e - b o d y A M w a s 9 % p - p o f

t h e a n i m a l ' s n o r m a l E O D m e a s u r e d w i t h in t h e c e l l 's r e -

c e p t i v e f ie l d . A d d i t i o n o f t h e l o c a l A M i n c r e a s e d t h e

m o d u l a t i o n a t t h e c e l l ' s r e c e p t i v e f i e l d t o 2 4 % p - p , a n d ,

i n i t i a l l y , t h e c e l l r e s p o n d e d v i g o r o u s l y . T h e l o c a l A M

w a s f i rs t a p p l i e d a t t h e p o i n t i n d i c a t e d b y t h e t o p o f t h e

b r a c k e t l a b e l e d B 2 o f F ig . 1 0 A a n d a p e r i o d h i s t o g r a m o f

t h e c e l l ' s r e s p o n s e s t o t h e f i r s t 2 0 p a i r e d l o c a l a n d

w h o l e - b o d y s t i m u l i i s s h o w n i n F i g . 1 0 B 2 . T h i s r e s p o n s e

d e c a y e d o v e r th e 2 0 0 s th a t th e p a i r e d s t i m u l i w e r e a p -

p l ie d ( c o m p a r e F i g . 1 0 B 2 ,B 3 ) a n d u p o n r e m o v a l o f th e

l o c a l A M , t h e c e l l s h o w e d t h e t y p i c a l n e g a t i v e i m a g e r e -

s p o n s e w h i c h a l s o d e c a y e d o v e r ti m e ( F i g . 1 0 B 4 , B 5 ) .

T h i s e x p e r i m e n t s h o w s t h a t p r o p r i o c e p t i v e i n p u t s a r e n o t

n e c e s s a r y f o r t h e p y r a m i d a l - c e l l p l a s t i c i t y ; e l e c t r o s e n s o -

r y i n p u t s a l o n e a r e s u f f i c ie n t . T h e s y s t e m c a n l e a r n t o r e -

j e c t l o c a l p a t t e r n s o f e l e c t r o s e n s o r y s t im u l i t h a t d i f f e r i n

a m p l i t u d e f r o m s t i m u l i r e c e i v e d o v e r l a r g e r r e g i o n s o f

t h e b o d y . C o n t r o l e x p e r i m e n t s v e r i f i e d t h a t t h e l o c a l A M

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

A M r e c e i v e d o v e r t h e r e s t o f th e a n i m a l ' s b o d y i f t h e

c a n c e l l a t i o n i s t o o c c u r .

I n o r d e r t o t e s t w h e t h e r t h e p r o p r i o c e p t i v e i n p u t s


10/16

72

Fig. 10 Raster disp lay (A) of a

basilar pyramidal cell s re-

sponses to an electronically

produced 0.4 Hz AM applied to

the whole body (section B1), to

this AM plus a local synchro-

nous AM applied to the cell s

receptive field (sections B2

through B3), and to the whole-

body AM presented alone fol-

lowing the paired stimuli (sec-

tions B4 through B5). B1-B5

Period histograms produced

from data of the raster display

indicated by the labeled brack

ets

B

1


B

3

B

4

B1

- 3 / 2 n 0 r d 2 r~ 3 / ' ~

2 5

0

-3 /2n

5 0 ~ =

2 5

0

-3 /2n

3 0

0 r d 2

n

3 / 2 n

0 ~ 2 n 3 / 2 n

15

- 3 / 2 ~

0 ~

n

3 /2 n

Am plitude m odulat ion phase

n ~ / 2 n

Fig. 11 Raster display (A) of

an ELL pyramidal cell s re-

sponses to +20 ~ 0.4 Hz tail

displacements recorded from

Eigenmannia

in the absence of

the animal s EOD (section B1).

Section B2 through B3 show

the cell s responses to the tail

displacement plus a local 0.4

Hz AM applied to the cell s re-

ceptive field and section B4

through B5 shows the cell s re-

sponse to the tail displacement

alone following the paired

stimulation. B1-B5 period his-

tograms produced from the da-

ta of the raster display indicat-

ed by the labeled brackets

, . . k -.. .~ p ~ - ~ r 1 6 2 - ~ p a ~

, . : ~ - - . . . ] t B

: . ~ ~ . ~ . . , , . .

9 . ..

L ' _ r ~ : ',

9 , " " . " r , # m ' . . ' ,

" " .%"~" " s 3

9 a, " - - "1 , , , i -

~ ~ . - . ~ . ~ . - ~ , ; ~ ~ . , t

: . ~ ~ ; '.~ . . - ~ - ' ~ Z . - ~ . ~

B1

3 0

15

0

+ 2 0

4 0

2 0

0

+ 2 0 0

4O

2O

0

+ 2 0 0

3 0 B J

1 5

0 -2 0 0 +2 0

-2 0

-2 0

~ ; , ~ . ~ . ~. ~ . ~ , ~ . .. . . . . 9 - . . 9 9 0+20 0 -20

9 , d e . ~ o - ; . u ~ ' . - . ~ Z l . , l Z , - ,. .,

~ t ~ - ' . ~ ~ - ~ . ~ : 8 " " . ~ . ~ . ' ~ L . . ~ 1 _

. f . ~ ; , . j ' . . - ~ - I ~ - . , I . . -. _ ' .; ,~ , = '. t .: J ,- - l- ~ , I d

s " " % . . ; . . :~ . . - , , ".

5

+ ao o - a o o + a o + 2 o o - a o

Tall displacement degrees)

+ 2 0

+ 2 0

+ 2 0

+ 2 0


11/16

J. Bastian: Pyramidal-cellplasticity

alone are also sufficient to support the pyramidal-cell

plasticity, the animal's electric organ discharge field

must be removed. Then local patterns of electrosensory

stimuli can be paired with tail displacements in the ab-

sence of the whole-body AMs normally resulting from

changes in posture. It is difficult to completely remove

the EOD of Apteronotus since this animal's electric or-

gan is composed of modified spinal motor neurons and

therefore insensitive to curare-like drugs. The related fish

Ei genmann i a was used instead, since its electric organ

discharge can be completely abolished via curarization.

The first segment of the raster of Fig. 1 I A, indicated by

the bracket labeled B 1, and the period histogram of these

data (Fig. llB1) show that this pyramidal cell was ini-

tially unresponsive to +20 ~ 0.4 Hz tail displacements.

During the second phase of this experiment (Fig. l lA,

sections B2 through B3) a local electrosensory stimulus

was applied to the cell's receptive field (+25 AM of a

400 laV, 300 Hz sinusoidal waveform). The cell's initial

response gradually became weaker over the 250 s that

the paired stimuli were applied (compare Fig. 11B2,B3).

Upon removal of the local AM, tail displacement alone

evoked a modulation of the cell's firing rate (negative

image) which decayed with continuous stimulation (Fig.

11B4,B5). This experiment shows that proprioceptive in-

formation alone, when paired with a local electrosensory

stimulus, also provides sufficient information for the

generation of pyramidal-cell plasticity.

iscussion

Proprioceptive inputs to the EGp

The presence of proprioceptive information within the

EGp, a structure intimately associated with the electro-

sensory system, is not surprising given that changes in

the animal's posture result in modifications in electro-

sensory input. The proprioceptive fibers recorded and la-

beled within the EGp of A. lep torhynchus show proper-

ties similar to fibers recorded and labeled within the EGp

of the mormyrid weakly electric fish, Gnat honemus pe -

tersii (Serrier et al. 1991), and proprioceptive responses

have also been recorded in dorsal granular ridge of el-

asmobranchs (Conley and Bodznick 1994). This struc-

ture is analogous to the EGp of gymnotiform and mo-

rmyriform fishes. High and regular firing rates and tonic

responses to changes in posture are typical of the pro-

prioceptive fibers seen in each of these animals, and in

all cases the axons of the granule cells receiving the pro-

prioceptive inputs, parallel fibers, project to the apical

dendrites of efferent neurons of the first-order sensory

processing area. These proprioceptive units have been

predicted to participate in mechanisms which somehow

identify, or reduce the consequences of, posturally gener-

ated electrosensory inputs (Bell et al. 1992; Szabo 1993;

Conley and Bodznick 1994).

The origin of the proprioceptive fibers in the gymnoti-

forms has not been determined. The intracellular labeling

73

of fibers in this study was never suffic iently complete to

identify the parent somata. Retrograde labeling experi-

ments of Sas and Maler (1987), and of this study, identi-

fied the lateral reticular nucleus as a major source of in-

put to the EGp, raising the possibility that proprioceptive

information may be relayed from the spinal cord via this

structure. Thus far, no studies have indicated that a direct

spinal projection to the EGp exists in gymnotiforms al-

though such a projection has been reported for the mo-

rmyrids along with projections via the anterior and pos-

terior lateral funicular nuclei and the lateral reticular nu-

cleus (Szabo et al. 1979; Szabo 1993). Additional ana-

tomical and physiological studies are needed to further

explore additional possible routes by which propriocep-

tive information might reach the EGp in gymnotiforms.

Receptor afferent and ELL pyramidal cell responses

The technique used in these studies to determine if pro-

prioceptive information influences ELL pyramidal cell

responses involved comparing a cell's responses to elect-

rosensory stimuli arising as a consequence of changes in

posture (tail-bend AMs) with responses to similar elect-

rosensory stimuli generated electronically without

changing the animal' s posture (mimic AMs). The validi-

ty of this comparison requires that the electronically pro-

duced stimulus is an accurate copy of the tail-bend AM.

The results summarized in Fig. 6 show that mimic ampli-

tudes and time courses are quite similar to those of tail-

bend AMs, and, as expected for equivalent stimuli, re-

ceptor afferents show no statistical difference in their re-

sponses to these. However, the agreement is not perfect;

some individual receptors responded differently to these

stimuli. This might result from using mimics imperfectly

matched in amplitude due to inaccurate measurement of

the voltage developed across the skin at the receptor site.

Pyramidal cell responses to AMs resulting from tail

displacement were significantly less than responses to

the mimics of these. In some cases a given cell was vir-

tually unresponsive to the tail-bend AM but clearly sen-

sitive to the mimic as shown in Fig. 7A,C. The average

pyramidal cell responses were about 70 stronger to

mimics as compared to tail-bend AMs even though aver-

age mimic amplitude was 10 smaller. This suggests

that central nervous system mechanisms exist which se-

lectively attenuate pyramidal cell responses to AMs that

result from changes in posture.

Only receptor afferents and ELL neurons with recep-

tive fields localized to the anterior 30 of the fish were

studied. Rostrocaudal variations in local EOD amplitude

are minimal over this region (Bastian 1981; Hoshimiya

et al. 1980; Rasnow et al. 1993), and EOD AMs due to

tail displacement are, therefore, expected to be homoge-

neous within this region. However, since EOD amplitude

was only measured at one site within a cell's receptive

field, I cannot eliminate the possibility that some spatial

variations in AM amplitude occurred. Such variations,

between the spatial distribution of the mimic AM and


12/16

74

tha t resu l t ing f rom ta i l d i sp lacemen t cou ld poss ib ly con-

t r ibu te to the d i f fe rences seen in py ramida l ce l l respons -

es.

Th e s i g n a l u s e d t o p ro d u c e t h e m i m i c A M w a s p r e -

sen ted t ransverse ly v ia e lec t rodes on e i ther s ide o f the

f i sh (F ig . 2 ,El ,E2) . Wi th th i s geomet ry , cu r ren t f low wi l l

be perpend icu lar to the sk in over the b road la te ra l su r -

f a c e o f t h e a n i m a l a n d u n i fo rm c h a n g e s i n EO D a m p l i -

t u d e a r e e x p e c t e d . S m a l l e r v o l t a g e s w i l l b e d e v e l o p e d

across the an imal ' s do rsa l and ven t ra l su r faces s ince cu r-

ren t f low i s t angen t ia l to the sk in in these reg ions . T here-

fo r e , t h e EO D A M s r e s u l t i n g f ro m t h e t r a n s v e r s e l y a p -

p l ied f i e ld a re expec ted to be smal le r in these do rsa l and

ven t ra l reg ions . The ampl i tude o f the d i scharge genera t -

ed by these an imals shows on ly a s l igh t decrease in am-

p l i tude a t more do rsa l and ven t ra l s i t es as compared to

s i t es on the body wal l (Rasnow e t a l . (1993) . Hence , the

p r inc ipa l spa t i a l var ia t ion expec ted in these exper imen ts

i s a reduced mimic AM ampl i tude res t r i c ted to the do rsa l

a n d v e n t r a l r e g i o n s o f t h e a n i m a l 's b o d y a s c o m p a re d t o

the AM genera ted by ac tua l changes in pos tu re . I t i s un -

l ike ly tha t th i s reduced mimic ampl i tude cou ld accoun t

fo r the s t ronger py ram ida l ce l l respons es to th i s s t imu lus .

Pyramida l -ce l l p las t i c i ty

As p roposed fo r o ther re la ted sys tems , py ramida l ce l l in -

sens i t iv i ty to the AMs resu l t ing f rom repe t i t ive t a i l d i s -

p l a c e m e n t s p ro b a b l y r e su l ts f r o m t h e s u m m a t i o n o f a

cen t ra l ly genera ted nega t ive ima ge (Bel l e t a l. 1993) o r

c a n c e l l a ti o n s ig n a l (B o d z n i c k a n d M o n t g o m e ry 1 9 9 4;

M o n t g o m e ry a n d B o d z n i c k 1 9 9 4 a ,b ) a n d t he r e c e p t o r a f-

fe ren t inpu t f rom the per iphery . Exper imen ts in wh ich

the pa t t e rn o f e lec t rosenso ry inpu t as soc ia ted wi th the

ta i l d i sp lacemen t i s sudden ly changed by add ing a spa-

t i a l ly loca l i zed AM (e .g . F ig . 8 ) show a g radual decay o f

the ce l l ' s in i t i a l response to the new s t imulus pa t t e rn .

The g radual reduc t ion in the ce l l ' s response i s a resu l t o f

t h e d e v e l o p m e n t o f t he n e g a t i v e i m a g e i n p ut w h i c h d e -

creases py ramida l ce l l exc i tab i l i ty a t t imes when in -

creased inpu t i s expec ted f rom the per iphery and increas -

es exc i tab i l i ty a t t imes decreased inpu t i s expec ted . Once

developed , the nega t ive image inpu t pers i s t s fo r a t ime

after the s t imulus is returned to i ts original pat tern .

Hence , py ramida l ce l l s show s t rong responses to an o r ig -

ina l ly inef fec t ive s t imulus pa t t e rn . These responses a re

mir ro r im ages o f the pa t t e rn tha t the ce l l had recen t ly

learned to re jec t . Th is cance l la t ion s igna l a l so decays

wi th con t inued s t imula t ion as the ce l l re learns to can -

ce l the cu rren t pa t t e rn o f a f fe ren t inpu t . Th is p las t i c char-

ac te r i s t i c enab les py ramida l ce l l s to dynamica l ly a l t e r

the i r sens i t iv i ty to repe t i t ive s t imul i . Pred ic tab le inpu ts

are thereby cance led , enhancing the ce l l s ' ab i l i ty to re -

spond to novel s t imul i .

Th e p l a s t i c d e v e l o p m e n t o f n e g a t i v e i m a g e s o r c a n -

c e l l a t i o n s i g n a l s i n g y m n o t i fo rm ELL p y ra m i d a l c e l l s

shares many s imi la r i t i es to e f fec t s seen in o ther sys tems .

In m o rm y r i d e l e c t r ic f i s h a c o ro l la ry o f t h e c o m m a n d

J. Bastian: Pyram idal-cell plasticity

s igna l wh ich u l t imate ly in i t i a tes the an imal ' s e lec t r i c o r -

gan d i scharge p ro jec t s to the EGp , and B el l (1981 , 1982 ,

1984, 1986, 1989), Bel l and Gran t (1989, 1992), and

Bel l e t a l . (1992 , 1993) have shown tha t the e f fec t s o f

th i s co ro l la ry d i scharge s igna l on ELL ce l l ac t iv i ty a re

p las t i c . The co ro l la ry d i scharge evokes pa t t e rns o f ac t iv i -

ty in ELL ce l l s tha t depend on the sys tem 's recen t s t imu-

la t ion h i s to ry and the e f fec t s o f th is inpu t op pose the e f -

fec t s o f repe t i t ive s t imul i rece ived f rom the per iphery .

Hence , the co ro l la ry d i scharge s igna l cance l s repe t i t ive

peripheral inputs .

M o re r e c e n t l y B o d z n i c k a n d M o n t g o m e ry (1 9 9 4 ) a n d

M o n t g o m e ry a n d B o d z n i c k (1 9 9 4 a ,b ) h a v e s h o w n t h a t

responses to e lec t rosenso ry s t imul i in ska tes and to no r-

mal lateral l ine s t imuli in scorpion fish are adapt ively fi l -

t e red o r re jec ted i f these a re coup led to the an imal ' s own

ven t i l a to ry movemen ts . The ce l l s s tud ied were found in

the f i r s t o rder e lec t rosenso ry and mechanosensory nu -

c le i , respec t ive ly , wh ich , as in the case o f the gymnot i -

fo rm and mormyrid ELL, rece ive para l l e l f iber inpu ts

f rom assoc ia ted popu la t ions o f g ranu le ce l l s . Bo th p ro -

p r iocep t ive inpu ts respons ive to ven t i l a to ry movemen ts

as wel l as co ro l la ry d i scharges o f ven t i l a to ry m oto r com -

mands p ro jec t to these g ranu le ce l l s (Con ley and Bodz-

n ick 1994 ; Montgomery and Bodzn ick 1994b) , and these

inpu ts a re the mos t l ike ly source o f the in fo rmat ion used

to genera te the cance l la t ion s igna ls .

Al l o f these s t ruc tu res showing senso ry p las t i c i ty in -

v o l v i n g t h e g e n e ra ti o n o f n e g a t iv e i m a g e s o f e x p e c t e d

inpu ts share impor tan t ana tomica l fea tu res and a l l a re

cerebe l la r - l ike in the i r o rgan iza t ion (Co om bs e t a l. 1993 ,

1994 ; M aler and M ugnain i 1993). Bel l e t a l. (1993) have

p ro p o s e d a m o d e l i n w h i c h t h e n e g a ti v e i m a g e o f a c e l l 's

expec ted recep to r a f fe ren t inpu t i s scu lp ted f rom the par -

a l l e l f iber inpu ts to i t s ap ica l dendr i t es , and long- te rm

d e p re s s i o n (LTD ) i s p ro p o s e d a s t h e c e l lu l a r m e c h a n i s m

under ly ing th i s p las t i c i ty . Montgomery and Bodzn ick

(1994a ,b ) p ropose a model , expressed as a se t o f l earn ing

ru les , wh ich shares impor tan t fea tu res wi th the Bel l e t a l .

m o d e l . Th e m e c h a n i s m s p ro p o s e d b y t h e s e a u t h o r s c a n

read i ly accoun t fo r the p las t i c i ty seen in th i s s tudy and

Fig . 12 summ arizes fea tu res o f these mode ls inco rpora t -

i n g t h e p ro p e rt i e s o f th e EL L o f Apteronotus

As a consequ ence o f ta i l d i sp laceme n ts , the py ramida l

ce l l s rece ive ascend ing e lec t rosenso ry inpu ts as wel l as

inpu ts to the ap ica l dendr i t es v ia the p ropr iocep t ive f i -

bers tha t p ro jec t to the EGp. Add i t iona l ly , the EGp re-

ce ives a descend ing e lec t rosenso ry inpu t f rom the n .

p raeeminen t ia l i s mul t ipo lar ce l l s . These neurons have

f i r ing p roper t i es s imi la r to those descr ibed fo r the p ro -

p r iocep t ive f ibers and the i r ton ic response charac te r i s t i c

a l l o w s t h e m t o a c c u ra t e l y e n c o d e t h e l o w - f r e q u e n c y

EOD AM resu l t ing f rom ta i l d i sp lacemen t . These mul t i -

po lar ce l l s a l so have l a rge b i l a te ra l recep t ive f i e lds and

are wel l su i t ed to encod ing spa t ia l ly ex tens ive changes in

EOD ampl i tude (Bas t i an and Bra t ton 1990) . The axons

o f b o t h t h e d e s c e n d i n g e l e c t ro s e n s o ry a n d p ro p r i o c e p t iv e

f ibers ramify ex tens ive ly wi th in the EGp p rov id ing inpu t

to many ind iv idua l g ranu le ce l l s . The g ranu le ce l l axons ,


13/16

J. B astian: Pyramidal-cell plasticity

Fig. 12 Diagram summarizing

mechanisms proposed to ac-

count for EL L pyramidal cell

insensitivity to repetitive elect-

rosensory inputs occurring

alone or together with changes

in the animal s posture.

Trian

g les and c i rc les indicate excit-

atory and inhibitory synapses,

respectively. See text fo r expla-

nation

otent ia l change E l e c t o r o s e n s o r y

ap ica l dendr i te

i npu ts

A 2 - - - ~ - ~ _ _ ~ . < ~

A 3 - - - . - ~ - - A

~ . / ~ ' - - - q ll

A 4

S l

otent ia l change

soma

S 2 _ _ , , .

s P y r a m i d a l c e l l

4 ~

S

P r o p . r i o c e p t i v e

i npu ts

9 A

E I

q v

T y p e I I

G r a n u l e

n e u r o n

7 5

P . I .

otent ia l change

bas i la r dendr i te

B 1

B 2 _ _ - - , . _ _

B 3

7

R e c e p t o r a f f e r e n t s

d o r s a l m o l e c u l a r l a y e r p a r a l l e l f i b e r s , e n t e r t h e D M L

over mos t o f i t s ro s t ro -caudal ex ten t and run fo r vary ing

d is tances w i th in the DM L (M aler e t al . 1974) . Very l a rge

n u m b e r s o f p a r a l l e l f i b e r s p ro b a b l y c o n v e y p ro p r i o c e p -

t ive and descend ing e lec t rosenso ry s igna l s to the py rami-

da l ce l l ap ica l dendr i t e as i l lu s t ra ted in F ig . 12 . The p ro -

p r iocep t ive and e lec t rosenso ry s igna l s car r i ed by ind iv id -

ua l para l l e l f ibers a re p resumed to have he te rogeneous

phase re la t ionsh ips . The type I and I I p ropr iocep t ive

f ibers respond to cyc l ic s t imul i rough ly in an t iphase

(F ig . 3) . Likewise , tw o ca tegor ies o f NP f ibers p ro jec t to

t h e EG p a n d t h e s e a r e e x c i t e d b y i n c r e a s e d a n d d e -

c r e a s e d EO D a m p l i t u d e , r e s p e c t i v e l y (B a s t i a n a n d B ra t -

ton 1990) . Di f fe ren t ia l de lays due to vary ing conduct ion

d is tances among para l l e l f ibers synaps ing on a g iven py-

ramida l ce l l shou ld fu r ther separa

bastian (1995) pyramidal-cell plasticity in weakly electric fish a mechanism for attenuating...

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