Expe imen al lesions o he eleos elencephalon impai asso-
cia i e lea ning in a a ie y o aining si ua ions. In he gold ish
(Ca assius au a us), o example, bila e al abla ions dis up he
acquisi ion o appe i i e isual condi ional disc imina ions (Onis-
hi, 1997), complex spa ial lea ning (Salas e al., 1996), he acqui-
si ion o a oidance beha io (Heinswo h e al., 1967), and he e-
en ion o p eope a i ely ained a oidance beha io (O e mie
and Papini, 1986). In e es ingly, bila e al lesions o he elencep-
halon do no lead o measu able dis up ion o lea ning in ela i ely
simple si ua ions, such as b igh ness disc imina ions (Onishi,
1997), escape condi ioning (Heinswo h e al., 1967), and a e si e
Pa lo ian condi ioning (O e mie and Cu now, 1969).
Resea ch on lea ning in animals sugges s ha o en a iables
ha ha e li le o no e ec s on he acquisi ion o new beha io s in
simple si ua ions, lead o signi ican e ec s when animals a e shi -
ed o ex inc ion. This is pa icula ly no iceable when p ac ice is
adminis e ed a a a e o a single ial pe day. Fo example, lesions
o he hippocampus in a s (Ja ad e al., 1964) o o he medial pa-
llium ( he amphibian homologue) in oads (Muzio e al., 1993; Pa-
pini e al., 1995) ha e no consequences o he acquisi ion o sim-
ple unning esponses ein o ced in all ials (i.e., con inuous ein-
o cemen , CR). Howe e , lesioned animals om bo h species
show abno mally high le els o pe sis ence du ing he ex inc ion
o ins umen al beha io . In e es ingly, he same lesion has oppo-
sing e ec s on ex inc ion when he ins umen al beha io was ac-
qui ed unde pa ial ein o cemen (PR). In a s, he hippocampal
lesion dec eases esis ance o ex inc ion (Ja ad e al., 1964; Ja ad
and Isaacson, 1965; Winocu and Mills, 1969), whe eas in oads,
lesions o he medial pallium inc ease esis ance o ex inc ion
(Muzio e al., 1993).
An in e es ing co olla y o his pa e n o esul s is ha i sug-
ges s ha PR aining engages di e en b ain p ocesses in a s and
oads. Hence, he lesion manipula ion has opposing e ec s on ex-
inc ion a e CR s. PR aining in a s (inc eased pe sis ence a -
e CR, bu dec eased pe sis ence a e PR), whe eas an equi alen
lesion manipula ion has he same e ec on ex inc ion in oads
(pe sis ence inc eased a e bo h CR and PR). Such di e ences in
he e ec s o physiological manipula ions a e consis en wi h he
hypo hesis, sugges ed by pu ely beha io al expe imen s, ha CR
and PR aining engage di e en lea ning p ocesses in mammals,
bu he same unde lying lea ning p ocess in o he e eb a es (Pa-
pini e al., 1995; Papini, 1997). One candida e media ional p ocess
in mammalian lea ning is p o ided by he hypo hesis ha pa ial
E ec o elencephalic abla ion on appe i i e ins umen al lea ning in
he gold ish (Ca assius au a us)
Emilio Du án, Juan P. Va gas, Cosme Salas and Mau icio R. Papini*
Uni e sidad de Se illa, * Texas Ch is ian Uni e si y
Gold ish ecei ed ei he bila e al abla ion o he elencephalon o a sham ope a ion, ollowed by ins-
umen al aining unde widely-spaced condi ions (one ial pe day). Animals we e ained o swim
in a unway o ei he con inuous ein o cemen o 50% pa ial ein o cemen . Thi y- wo daily acqui-
si ion sessions we e ollowed by 32 daily ex inc ion sessions du ing which ood was wi hheld. Telen-
cephalic lesions dis up ed ea ly acquisi ion pe o mance, bu lesioned animals achie ed an asymp o ic
pe o mance simila o ha o sham con ols. Ex inc ion was acili a ed by he lesions, independen ly
o he schedule o ein o cemen used du ing acquisi ion. The esul s a e in e p e ed in ela ion o com-
pa a i e esea ch on spaced- ial appe i i e ins umen al lea ning in e eb a es.
E ec os de la ablación elence álica sob e el ap endizaje ape i i o ins umen al en la ca pa do ada
(Ca assius au a us).En es e expe imen o se emplea on ca pas do adas (Ca assius au a us) con abla-
ción bila e al del elencé alo o con ope ación de con ol en un p ocedimien o de en enamien o ins u-
men al con dis ibución de ensayos ampliamen e espaciados (un ensayo po día). Los animales ue on
en enados a nada en un co edo bajo condiciones de e o zamien o con inuo o e o zamien o pa cial
al 50%. Se ealiza on 32 sesiones dia ias de adquisición seguidas de 32 sesiones dia ias de ex inción
en las que la comida ue sup imida. La lesión elence álica a ec ó a la adquisición du an e los p ime-
os ensayos aunque, al inal, los animales lesionados alcanza on una ejecución asin ó ica simila a la
de los animales con oles. La ex inción se io acili ada po las lesiones, independien emen e del p o-
g ama de e o zamien o usado du an e la adquisición. Los esul ados se in e p e an en elación a los
es udios compa a i os de ap endizaje ins umen al ape i i o con ensayos espaciados ealizados en
o os e eb ados.
Co espondencia: Emilio Du án Ga cía
Depa amen o de Psicología Expe imen al
Facul ad de Psicología
41005 Se illa (Spain)
E-mail: [email p o ec ed]
Psico hema ISSN 0214 - 9915 CODEN PSOTEG
2000. Vol. 12, nº 4, pp. 520-524 Copy igh © 2000 Psico hema
ein o cemen induces he ac i a ion o an emo ional eac ion o
us a ion elici ed by he su p ising omission o an appe i i e ein-
o ce (G ay, 1987; Amsel, 1992; Papini and Dudley, 1997). The
p esen expe imen was designed o de e mine i a global lesion o
he ish elencephalon a ec s he ex inc ion o widely-spaced ins-
umen al lea ning in he same di ec ion (as in amphibians), o in
opposi e di ec ion (as in mammals), as a unc ion o whe he ac-
quisi ion in ol ed CR o PR.
Me hod
Subjec s
The subjec s we e 32 expe imen ally nai e gold ish (Ca assius
au a us) pu chased om a local aqua ium in Se ille. Gold ish we-
e 12-15 cm in body leng h and li ed in pai s in anks measu ing
42 x 26 x 15 cm. Tanks we e cleaned e e y 2 days. Wa e was kep
a a cons an empe a u e o 21°C and con inuously ae a ed. The
aqua ium oom was kep unde a 14:10 h ligh : da k cycle (ligh
om 07:00 h o 21:00 h ). Ex ensi e handling expe ience was ad-
minis e ed du ing he 60 days p io o he ini ia ion o he aining
sessions. Gold ish we e indi idually handled on a daily basis. Be-
ginning 3 weeks be o e he expe imen , a daily eeding ou ine
was in oduced. Each gold ish was gi en 3 pelle s o Te a-pond
(Ul ich Baensch GmbH, Ge many) ish ood (a o al o abou 0.08
g o ood pe day).
Appa a us
Animals ecei ed aining in a con en ional unway made ou
o whi e ac ylic pla es. The unway was 150 cm long X 10 cm wi-
de X 15 cm high, and was di ided in o h ee sec ions. The s a and
goal boxes we e 25 cm long. Manually-ope a ed guillo ine doo s
sepa a ed he s a and goal boxes om he main sec ion o he
unway. A ube measu ing 8-mm in diame e was loca ed in he
goal box and used o manually deli e he ood on ein o ced
ials. The unway was illed wi h wa e up o a le el o 12 cm.
Wa e was cons an ly ci cula ing om he s a o he goal box.
Opening o he s a doo ac i a ed a digi al coun e (inc emen ing
in 0.01 s uni s) ha was s opped when he animal ac i a ed a pho-
ocell loca ed inside he goal box. The la ency o a e se he un-
way was he p ima y dependen measu e.
Su gical and His ological P ocedu es
Animals we e anes he ized by imme sion in a solu ion o i-
caine me hanosul ona e (1:20,000). When mo emen ended, he
animal was placed in he su gical chambe whe e i emained pa -
ially ba hed in wa e a a cons an concen a ion o anes he ic
(1:20,000). The animal was ixed in o posi ion by la e al holde s
ha main ained he body s ill du ing su ge y. An adjus able ube
was inse ed in o he animal’s mou h and connec ed o a pump ha
p o ided a cons an low o wa e . The concen a ion o anes hesia
was kep cons an du ing su ge y.
The do sal skin and skull we e ca e ully emo ed and he un-
de lying a y issue emo ed by aspi a ion. The exposed elencep-
halon was aspi a ed wi h a mic opipe e connec ed o a manual a-
cuum sys em. Su ge y was pe o med unde isual inspec ion by
means o a binocula mic oscope. Following he abla ion, he pie-
ce o skull was eplaced in i s o iginal posi ion, ixed wi h cyano-
c ila e glue, and co e ed wi h den al cemen . The ish was hen e-
u ned o i s home ank o a eco e y pe iod o 6 days. Sham ope-
a ions we e pe o med exac ly as desc ibed, excep ha he ne -
ous issue was no inju ed.
A he end o he expe imen , ish we e deeply anes he ized
(1:5,000) and pe used wi h 50 ml o 0.9% saline solu ion, ollo-
wed by 125 ml o ixa i e solu ion (10% o malin in phospha e
bu e 0.1 M, pH 7.4). The b ains we e emo ed om he skull,
inspec ed o a p elimina y e alua ion o he abla ion, and cu in
50-mm hick ans e sal sec ions o his ological analysis.
T aining P ocedu e
All ish ecei ed 7 daily sessions o p e aining immedia ely a -
e he 6 days o pos -su gical eco e y. Du ing he ini ial 5 ses-
sions, each animal was exposed o he unway appa a us wi h he
doo s aised and wi hou any ood o a o al o 5 min pe session.
Du ing sessions 6 and 7, each gold ish was con ined o 5 min o
he goal box o he unway whe e i ecei ed a o al o 6 pelle s o
Te a-pond ish ood (app oxima ely 0.15 g).
T aining begun on day 8. Sham-ope a ed and abla ed animals
we e andomly assigned o one o wo g oups. G oups C/S and P/S
included sham-ope a ed (S) animals ha ecei ed ei he con i-
nuous ein o cemen (C) o 50% pa ial ein o cemen (P) aining.
G oups C/L and P/L included lesioned (L) animals ecei ing he
same aining schedule. Acquisi ion las ed 32 daily ials and he
in e ial in e al was app oxima ely 24 h . All he ials in he C
g oups ended in ein o cemen , wi h he deli e y o 6 pelle s o Te-
a-pond ish ood (abou 0.15 g). Fo he g oups ecei ing 50%
pa ial ein o cemen , 16 ials ended in ein o cemen , while he
es ended in non ein o cemen . The sequence o ein o ced (R)
and non ein o ced (N) ials was he ollowing: RNRRN RNRNN
RNNRN RNRRN RNNRR NNRNR RN. Ex inc ion begun he
day a e he las acquisi ion ial and las ed ano he 24 daily ials,
all non ein o ced.
Animals we e anspo ed om hei home ank in o he s a
box o he unway. A e 20 s, he s a doo was aised and he ial
s a ed. The ial ended when he ish in e up ed he pho ocell lo-
ca ed in he goal box. I he ial was ein o ced, he ood was ad-
minis e ed immedia ely a e he pho ocell was ac i a ed and he
animal was gi en 20 s o consume he ood. In a non- ein o ced
ial, animals we e le in he goal box du ing 20 s a e he pho o-
cell was ac i a ed. Animals we e e u ned o hei home anks im-
media ely a he end o each ial. Pos - ial supplemen a y eeding
(6 pelle s, abou 0.15 g) was p o ided o hose animals exposed
o an N ial, ei he du ing pa ial ein o cemen aining o du ing
ex inc ion, 30 min a e he end o he ial. The o de in which ani-
mals ecei ed aining in any gi en day was de e mined as ollows:
squads o 4 gold ish, one om each g oup, we e un always in he
same o de , bu he o de o aining wi hin a pa icula squad was
changed andomly ac oss days.
Resul s
Th ee lesioned animals died in he cou se o he ex p e i m e n .
In addi ion, one ish in G oup P/S ailed o comple e 5 o he las
8 acquisi ion ials and exhibi no clea e idence o acquisi ion.
G i en he emphasis on ex inc ion pe o m a n c e, his animal wi h
a poo acquisi ion e c o d was disca ded om he s udy. Only h-
ee o he go l d ish ailed o inish a ial (one animal in G oup C/S
EFFECT OF TELENCEPHALIC ABLATION ON APPETITIVE INSTRUMENTAL LEARNING IN THE GOLDFISH… 521
ailed in wo ials, and wo animals in G oup P/L ailed in one
ial each, ou o a o al o 32 acquisi ion ials). Because hese
we e isola ed a i l u es, hese animals we e kep in he analy s e s .
Th e e we e, hus, 4 a i l u es ou o a o al o 896 acquisi ion i a l s
( o n ly 0.4% dis up ion). The inal g oup sizes we e he o l l ow i n g :
G oup C/S, n=8; G oup C/L , n=7; G oup P/S, n=7, and G o u p
P/L, n=6.
Fi g . 1 shows he ex en o he elencephalic issue e m o al in
ep e s e n a i e b ains. The lesion esul ed in he comple e e m o-
al o he elencephalic lobes. The p eop ic a ea and he op ic
ac s we e no inju ed in any o he animals subjec ed o su ge y.
None o he sham ope a ed go l d ish exhibi ed damage o he
b a i n .
L a e n cy sco es ob ained o each animal, in each ial, we e
a n s o med o he log 1 0 o he pu pose o imp o ing no m a l i y
and allowing o pa a m e ic analysis o he esul s. The e s u l s
a e shown in Fi g. 2. Ea ly acquisi ion pe o mance was poo e in
bo h lesioned g oups han in he sham con ols, bu he lesioned
animals e e n u a l ly e a ched a simila (P/L) o be e (C/L) beha-
i o al le el han hei e s p e c i e sham con ols. Th e e was a
small bu consis en dec ease in la encies in he wo sham-ope a-
ed g oups. Howe e , he e was no ob ious e ec o he sch e d u-
le o e i n o cemen . A Schedule (C, P) x Lesion (L, S) x 4-T i a l
B l o ck analysis o a iance on he a n s o med la encies yielded
a signi ican acquisi ion e ec [F(7, 168) = 5.339, p < 0.001], a
s i g n i ican Lesion x T ial in e ac ion [F(7, 168) = 5.835, p <
0.001], and a signi ican main e ec o lesion [F(1, 24) = 4.845,
p < 0.04].
Fu he pai wise compa isons wi h he e o e m and d de i-
ed om he main analysis (Howell, 1992) we e compu ed o e
he las wo 4- ial blocks o acquisi ion in o de o de e mine
whe he he g oup di e ences we e signi ican . Non-signi ican
di e ences we e ound in Blocks 7 and 8 be ween G oups C/S and
C/L [Fs(1, 87) < 3.851, all p > 0.05] and be ween G oups P/S and
P/L [Fs(1, 87) < 1, all p > 0.05].
Fi g. 2 also shows ha bo h lesioned g oups exhibi ed less
p e sis ence in ex inc ion han each o hei e s p e c i e sham con-
ols. This pa e n sugges s ha he elencephalic lesion a e c e d
ex inc ion in he same manne whe he he esponse was acqui-
ed ia con inuous o pa ial e i n o cemen a i n i n g. Th e e wa s
also a endency o he wo g oups ained unde pa ial e i n o -
cemen o exhibi highe la encies han hose o he g oups a i -
ned unde con inuous e i n o cemen . A Schedule (C, P) x Le-
sion (L, S) x 4-T ial Block analysis o a iance on he a n s o -
med la encies con i med bo h obse a ions. Th e e was a signi i-
can lesion by bl o ck in e ac ion [F(7, 168) = 2.292, p < 0.03],
and a signi ican main e ec o schedule [F(1, 24) = 4.349, p <
0 . 0 5 ] .
Al hough he asymp o ic acquisi ion pe o mance o hese
g oups was s a i s i c a l ly simila , i is ob ious ha he go l d ish in
G oup C/L s a ed ex inc ion a lowe la e n cy le els han he
o he g oups. In o de o assess ex inc ion a e indep e n d e n l y o
he s a ing poin , he ex inc ion la encies we e e - c a l c u l a ed by
using a e l a i e measu e. The log1 0 l a e n c y sco e o each ani-
mal, in each ex inc ion ial, was a n s o med acco ding o he
o mula: ( ial / asymp o e) x 100, wh e e asymp o e was he
mean log1 0 s c o e o ha animal du ing he las 8 acquisi ion
ials. T a n s o med sco es we e a e aged in bl o cks o 4 i a l s
o each animal. Thus, sco es ab o e 100 ep esen an inc e a s e
in la e n cy du ing ex inc ion, e l a i e o asymp o ic acquisi ion
p e o m a n c e.
The esul s a e p esen ed in Fig. 3. The e was subs an ially mo-
e change in beha io du ing ex inc ion, ela i e o he las 8 ac-
quisi ion ials, in G oups C/L and P/L han in hei ela i e sham
con ols, C/S and P/S. The e was also a g ea e a e age change in
he pa ial ein o cemen g oups han in he g oups ha had ecei-
ed con inuous ein o cemen aining. A Schedule (C, P) x Lesion
(L, S) x 4-T ial Block analysis o a iance on he ans o med sco-
es yielded a signi ican lesion by block in e ac ion [F(7, 168) =
2.307, p < 0.03], con i ming ha he ex inc ion pe o mance o he
lesioned g oups ex inguished signi ican ly as e han ha o he
sham con ols. The e was also a bo de line lesion e ec [F(1, 24)
= 4.072, p = 0.0549]. All o he e ec s we e non-signi ican , inclu-
ding he schedule e ec s.
EMILIO DURÁN, JUAN P. VARGAS, COSME SALAS AND MAURICIO R. PAPINI
522
Figu e 1. T ans e se pos commissu al sec ion o a no mal b ain (A) and a elencephalon-abla ed b ain (B). DC, cen al a ea o he do sal elencephalon;
DD, do sal a ea o he do sal elencephalon; DL, la e al a ea o he do sal elencephalon; DM, medial a ea o he do sal elencephalon; OC, op ic chiasm;
PO, p eop ic nucleus; PP, pe i en icula p eop ic nucleus; c, ela cho oidea; V, en icle.
Discussion
Wi d e ly-spaced ex p e imen s on ins umen al lea ning wi h
go l d ish sugges ha beha io is s eng hened by e i n o c e m e n
and we a kened by non e i n o cemen (Lowes and Bi e m a n ,
1967). Unlike i is he case wi h mammals, go l d ish da a, as we l l
as he esul s o analogous ex p e imen s wi h oads and u l e s
( Pe and Bi e man, 1970; Muzio e al., 1993; Papini and Ishida,
1994 ), do no e q u i e he assump ion ha he su p ising omis-
sion o educ ion in ewa d quan i y o quali y induces an emo-
ional eac ion o u s a ion (G ay, 1987; Amsel, 1992; Pap i n i
and Dudley, 1997). In ag eemen wi h p e ious ex p e imen s, he-
e was no e idence o g e a e esis ance o ex inc ion a e PR ac-
quisi ion, a he han CR acquisi ion, in he sham g oups. Th i s
was he case whe he ex inc ion was assessed in e ms o ab s o l u-
e o a n s o med la encies. The absence o a ma ked pe o m a n-
ce ch a n ge du ing ex inc ion in he sham g oups may appea unu-
sual. Howe e , i is no uncommon o go l d ish ained unde wi-
d e ly-spaced condi ions o exhibi subs an ial pe sis ence o ins-
umen al beha io du ing ex inc ion (Boi ano and Fo s ke , 1968;
S c hu z and Bi e man, 1969).
Lesion ex p e imen s can con i bu e o de e mine whe he be-
h a i o al di e ences ac oss species e lec di e ences in he un-
d e lying p ocesses o ins umen al lea n i n g. I CR and PR a i-
ning lead o he same unde lying ype o lea n i n g, as i is hy p o -
h e s i zed o be he case in he go l d ish, hen abl a ion o a pa i c u-
la a ea known o be in o l ed in lea ning should lead o he sa-
me ex inc ion e ec in bo h aining condi ions. The p esen e-
sul s demons a e ha he comple e abl a ion o he elencep h a-
lon, a s u c u e known o be in o l ed in lea ning in eleos i s h
( O e mie and Hollis, 1990), leads o educed esis ance o ex-
inc ion indep e n d e n ly o whe he he esponse was acqui ed un-
de CR o unde PR a i n i n g.
Conclusions
(1) Pa ial ein o cemen aining does no inc ease esis ance
o ex inc ion in he gold ish.
(2) A bila e al lesion o he elencephalon does no a ec ac-
quisi ion pe o mance, bu i educes esis ance o ex inc ion simi-
la ly in animals ained unde pa ial o con inuous ein o cemen .
Acknowledgmen s
The esea ch epo ed he e was suppo ed in pa wi h g an s
om he DGES PB96-1334 and Jun a de Andalucía CVI-242. The
au ho s wish o hank Ge a do Lab ado o his echnical help in
p epa ing he mic opho og aphs.
EFFECT OF TELENCEPHALIC ABLATION ON APPETITIVE INSTRUMENTAL LEARNING IN THE GOLDFISH… 523
4-Session Blocks
1,8
1,6
1,4
1,2
1,0
0,8 0246810 12 14 16
Acquisi ion Ex inc ion
CL
CS
PL
PS
Figu e 2. Pe o mance o g oups o gold ish ained unde ei he con i -
nuous (C) o pa ial (P) ein o cemen du ing acquisi ion, and subjec o
elencephalic lesion (L) o sham ope a ion (S) be o e he s a o aining.
Expe imen o 2
Causas
A
64,54
39,76
B
68,72
35,54
D
74,06
30,1
C
65,38
45,1
Usual
Ra a
100
80
60
40
20
0
Figu e 3. Ex inc ion pe o mance o g oups ained unde con inuous (C)
o pa ial (P) ein o cemen du ing acquisi ion, and subjec o a elencep -
halic lesion (L) o a sham ope a ion (S) be o e aining. La encies (s) om
each ial we e ans o med o hei log10 alue be o e compu ing he pe -
cen age o change. The log10 alue o each ex inc ion ial was di ided by
he a e age log10 alue o he las 8 sessions o acquisi ion and he a io
mul iplied by 100. Change abo e 100 implies longe la encies in ex inc ion
han du ing asymp o ic acquisi ion.
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P ess.
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speed o app oach esponses in gold ish (Ca assius au a us). Psycho -
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Heinswo h, F. R.; O e mie , J. B.; Snowdon, C. T. (1967). Speci ic and
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524
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