Beha io al/Sys ems/Cogni i e
A oidance Response in Gold ish: Emo ional and Tempo al
In ol emen o Medial and La e al Telencephalic Pallium
Manuel Po a ella,
1
Blas To es,
2
and Cosme Salas
1
1
Labo a o io de Psicobiologı´a, Depa amen o de Psicologı´a Expe imen al, Uni e sidad de Se illa, E-41018 Se ille, Spain, and
2
Labo a o io de
Neu obiologı´a, Depa amen o de Fisiologı´a y Zoologı´a, Uni e sidad de Se illa, E-41012 Se ille, Spain
Thehippocampusand heamygdalaa ein ol edina oidancelea ninginmammals.Themedialandla e alpalliao ac inop e ygian ish
ha e been p oposed as homologous o he mammalian pallial amygdala and hippocampus, espec i ely, on he basis o neu oana omical
indings. This wo k was aimed a s udying he e ec s o abla ion o he medial elencephalic pallia (MP) and la e al elencephalic pallia
(LP) in gold ish on he e en ion o a condi ioned a oidance esponse p e iously acqui ed in wo expe imen al condi ions. In he i s
expe imen , ish we e ained in non ace a oidance condi ioning. In he second expe imen , ish we e ained in ace a oidance
condi ioning in which empo al cues we e c ucial o he lea ning p ocess. An MP lesion a ec ed he e en ion o he a oidance esponse
in bo h p ocedu es; in con as , an LP lesion impai ed he e en ion only in he ace-condi ioning p ocedu e. These da a suppo he
p esence o wo di e en sys ems o memo y in ish, based on disc e e elencephalic a eas: he MP, in ol ed in an emo ional memo y
sys em;and heLP,in ol ed inaspa ial, ela ional,o empo al memo ysys em.Mo eo e , hesedi e en iale ec s we esimila o hose
p oduced by amygdala and hippocampal lesions in mammals. We conclude ha hese specialized sys ems o memo y could ha e
appea ed ea ly du ing phylogenesis and could ha e been conse ed h oughou e eb a e e olu ion.
Key wo ds: amygdala; hippocampus; a oidance lea ning; memo y sys ems; elencephalon; b ain e olu ion; eleos ish
In oduc ion
In mammals, he amygdala and hippocampal sys ems accom-
plish an impo an ole in he acquisi ion and e en ion o con-
di ioned a oidance esponse (McIn y e and S ein, 1973; G oss-
man e al., 1975; Sa´nchez-Riolobos, 1986; Rawlins e al., 1993;
Winocu , 1997). The amygdala is in ol ed in emo ional beha -
io s and emo ional memo y (LeDoux, 1995). I is also in ol ed in
a oidance lea ning because lesions o amygdala nuclei abolish he
acqui ed condi ioned esponse (Sa´nchez-Riolobos, 1986;
Amb ogi-Lo enzini e al., 1991). I is known ha hippocampal
and sep al lesions acili a e a oidance lea ning in mammals in
some ci cums ances (O’Kee e and Nadel, 1978; Sa a and Da id-
Remacle, 1981; G ay and McNaugh on, 1983; Weine e al.,
1998). Howe e , hese lesions p oduce ha m ul e ec s when he
con ex ual o ime cues a e signi ican o he condi ioning p o-
cess, as in he case o a oidance lea ning o ace emo ional con-
di ioning p ocedu es (Wood u and Kan o , 1983; Moye e al.,
1990; Phillips and LeDoux, 1992). Thus, he hippocampus is in-
ol ed in spa ial lea ning (O’Kee e and Nadel, 1978), in ela ional
memo y (Eichenbaum e al., 1992; Squi e, 1992), and in he p o-
cessing o empo al a ibu es o e en s and si ua ions (Kesne
and DiMa ia, 1987).
In ac inop e ygian ish, he la e al elencephalic pallium has
been p oposed as homologous o he hippocampus on he basis
o bo h neu oana omical e idence (Nieuwenhuys and Meek,
1990; B a o d, 1995; No hcu , 1995; Bu le , 2000) and he in-
ol emen o his a ea in place lea ning by means o allocen ic
ames o e e ence (Rod ı´guez e al., 2002). The medial pallium
has been p oposed as homologous o pallial amygdala (Ma ino-
Ne o and Sabba ini, 1983; Nieuwenhuys and Meek, 1990;
B a o d, 1995; No hcu , 1995; Bu le , 2000).
The beha io al na u e o he condi ioned a oidance esponse
in e apods has been explained by means o he wo-p ocess
heo y o Mow e (1960). In e es ingly, comple e elencephalic
abla ion in ish p oduces de as a ing e ec s on he acquisi ion
and main enance o a wo-way condi ioned a oidance esponse
(O e mie and Papini, 1985, 1986; Papini, 1985; O e mie and
Hollis, 1990). Flood e al. (1976) p oposed, on he basis o Mow-
e ’s heo y, ha he unc ion o he ish elencephalon is o use
he emo ional s a es as condi ioned ein o ce s o p oduce in-
s umen al esponses. Abla ion o he elencephalon he e o e
dis up s a oidance condi ioning because i p e en s engagemen
be ween wo p ocesses o lea ning (Pa lo ian and ins umen al).
Fu he mo e, i is p obable ha es ic ed elencephalic a eas will
be di ec ly in ol ed in his unc ion as a pa o a ious special-
ized sys ems o memo y, as has been p oposed in land e eb a es
(Schac e and Tul ing, 1994).
The aims o his wo k we e o de e mine whe he medial and
la e al pallium lesions in eleos ish p oduce di e en ial e ec s
on he e en ion o he a oidance esponse p e iously acqui ed in
Recei ed No . 4, 2003; e ised Jan. 14, 2004; accep ed Jan. 17, 2004.
This esea ch was suppo ed by Spanish Minis e io de Ciencia y Tecnologı´a G an s BF I2001-3178, I2000-0315,
I2003-0029, PB 96-1334) and Jun a de Andalucı´a CVI-242. We hank M. T. Gu ie´ ez, G. Lab ado , and E. Cue os o
echnical assis ance.
Co espondence should be add essed o Manuel Po a ella, Labo a o io de Psicobiologı´a, Depa amen o de
Psicologı´aExpe imen al, Facul addePsicologı´a,Uni e sidad deSe illa,C/CamiloJose´ Cela s/n,41018Se ille,Spain.
E-mail: [email p o ec ed].
DOI:10.1523/JNEUROSCI.4930-03.2004
Copy igh © 2004 Socie y o Neu oscience 0270-6474/04/242335-08$15.00/0
The Jou nal o Neu oscience, Ma ch 3, 2004 •24(9):2335–2342 • 2335
wo di e en si ua ions ( wo-way ac i e a oidance condi ioning
and ace wo-way ac i e a oidance condi ioning), o es
whe he hese sepa a e pallial a eas sha e unc ional simila i ies
wi h hei mammalian b ain homologues, and o analyze he
possible p esence o mul iple elencephalon-based memo y sys-
ems in ish.
Ma e ials and Me hods
Expe imen 1: wo-way ac i e a oidance condi ioning
As desc ibed abo e, he ish medial and la e al pallia ha e been p oposed
as homologous o he mammalian pallial amygdala and hippocampus,
espec i ely (Nieuwenhuys and Meek, 1990; B a o d, 1995; No hcu ,
1995; Bu le , 2000). Va ious expe imen s ha e shown ha he la e al
pallium has unc ional implica ions in spa ial lea ning, simila ly o he
hippocampus (Va gas e al., 2000; Rod ı´guez e al., 2002), and o he s
sugges he p esence o a elencephalon-based emo ional lea ning sys em
in ish (Po a ella e al., 2003). The aim o his expe imen was o de e -
mine whe he speci ic damage o he medial o la e al pallium could
p oduce di e en ial de ici s in wo-way a oidance condi ioning in gold-
ish, simila o hose caused by damage o pallial amygdala and hip-
pocampus, espec i ely. An expe imen o wo-way a oidance condi-
ioning was pe o med using a p e ious design o a ish shu le box
(Ho ne e al., 1961). The p esen a ion o shock (used as an a e si e
s imulus) was comple ely o e lapped wi h a p e ious g een ligh p esen-
a ion (used as a disc imina i e s imulus) o minimize he in e s imulus
empo al ac o .
Subjec s
Fo y expe imen ally nai e gold ish, pu chased om a local supplie (in
Se ille), se ed as subjec s in his expe imen . The animals we e be ween
9 and 11 cm in body leng h and we e housed in small g oups in glass
aqua ia (200 l) wi h ae a ed and il e ed wa e a a cons an empe a u e
o 20°C. The aqua ium oom was subjec o a 14/10 h ligh /da k cycle
(ligh s on om 7 A.M. o 9 P.M.). Pelle s o d y ood (Te a-Pond; Ul ich
Baemsch GmbH, Melle, Ge many) we e p o ided daily ad libi um du ing
he expe imen al pe iod. The expe imen al manipula ions desc ibed in
his a icle we e conduc ed in acco dance wi h Di ec i e 86/609/CEE o
he Eu opean Communi y Council and Spanish Real Dec e o 223/1988.
Appa a us
Fou simila shu le boxes we e used, ollowing a p e iously desc ibed
design (Ho ne e al., 1961) (Fig. 1). Each shu le box consis ed o a
wa e - illed glass ank (50 ⫻25 ⫻14 cm). Black poly inyl chlo ide
(PVC) co e ed each long side; he loo was co e ed wi h whi e PVC; and
he wo box ends we e clea and anslucen o pe mi he g een ligh
p esen a ion as a disc imina i e s imulus (10 W, 220 V AC, 50 Hz). On
each long side, wo s ainless s eel ba s a ached o me al pla es we e used
as elec odes o deli e a uni o m, mild elec ic shock as an a e si e
s imulus (0.39 V/cm, 50 Hz, pulsed 200 msec on and 800 msec o ). A
apezoidal ba ie (7.5 cm high, 10 cm wide a he op, and 18 cm wide a
he bo om) di ided he shu le box in o wo compa men s. On he
ba ie , wo pai s o pho oemi e s ( ed ligh s, 24 V DC, 0.3 W) and
pho o ecep o s (pho o esis o s, 3 V cc) de ec ed he ish shu le e-
sponses ac oss i . The wa e le el o e he ba ie was kep cons an a 2
cm, gi ing a wa e le el o 9.5 cm in each o he compa men s. The wa e
was ae a ed con inuously. The shu le boxes we e con olled by a com-
pu e ized sys em (Le ica SL) o a condi ioning, adap ed and modi ied
in ou labo a o y. The so wa e d i ing he shu le boxes (Skinne ; Cib-
e ec SA) was also adap ed o deli e he s imuli and o eco d he ish
esponses.
P ocedu e
P eexposu e. Be o e aining sessions, ish we e p eexposed indi idually
o he expe imen al appa a us on 3 consecu i e days. On he i s day, he
animals we e placed in he shu le box wi h he wa e le el se a 6 cm
abo e he ba ie and we e allowed o swim eely h ough he appa a us
o 30 min wi hou any s imulus p esen a ion. Fo he ollowing wo
sessions, each o 5 min, he wa e le el was d opped o 2 cm abo e he
ba ie ; he animals did no ecei e condi ioning s imuli.
Acquisi ion. All animals we e ained using he same p ocedu e. This
consis ed o daily sessions o 10 ials sepa a ed by an in e ial in e al
(ITI) o a ying du a ion, anging be ween 1 and 2 min. A he end o he
ITI, he ial began. The disc imina i e s imulus was u ned on o a
maximum du a ion o 15 sec in he compa men whe e he ish was
loca ed. I he ish did no espond (swimming ac oss he ba ie ) wi hin
10 sec o g een ligh onse , he elec ic shock was u ned on o a maxi-
mum o 5 sec. Thus, he empo al sepa a ion be ween cue onse and
shock onse was 10 sec. A esponse du ing he i s 10 sec inished he
wa ning s imulus (g een ligh ), and he shock was no deli e ed. A e-
sponse du ing he 10–15 sec pe iod canceled bo h he wa ning s imulus
and he shock. Be o e s a ing and a e inishing he daily aining ses-
sion, he subjec es ed in he shu le box o 5 min wi hou any s imulus
p esen a ion. The animals we e ained un il hey eached he lea ning
c i e ion, o a maximum o 20 sessions. I an animal had no eached he
c i e ion in his pe iod, i was ejec ed om he expe imen . A lea ning
c i e ion was es ablished o a leas 70% o a oidance esponses in i e o
six consecu i e aining sessions (O e mie and Papini, 1986). All sub-
jec s eached he c i e ion be ween sessions 8 and 15 and we e andomly
assigned o one o i e g oups: medial pallium (MP) abla ion (n⫽8),
la e al pallium (LP) abla ion (n⫽8), elencephalon (TEL) abla ion (n⫽
8), sham-ope a ed (n⫽8), and con ol (n⫽8). The a iables eco ded
o he c i e ion sessions we e la ency o esponses and pe cen age o
a oidance (shu le esponses occu ing be o e shock onse ; he la ency
was ⬍10 sec) and escape (shu le esponses occu ing du ing he shock;
he la ency was be ween 10 and 15 sec). ANOVA wi h epea ed measu e-
men s was used o s a is ical analysis.
Su ge y. A e he acquisi ion phase, ish we e anes he ized by imme -
sion in a 1:20,000 solu ion o icaine me hane sul ona e (Sigma, S .
Louis, MO) wi h cons an low o ae a ed wa e h ough he gills. The
animal was hen placed in he su gical chambe , whe e i emained ixed
in place by la e al holde s and pa ially ba hed in wa e . 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 wi h a cons an concen a ion o anes-
he ic du ing su ge y.
The do sal skin and skull we e ca e ully emo ed, and he unde lying
a y issue was emo ed by aspi a ion. The elencephalic issue was as-
pi a ed ca e ully wi h a mic opipe e connec ed o a manual acuum
sys em. Su ge y was pe o med unde isual inspec ion by means o a
binocula mic oscope. The sulcus ypsili o mis, sulcus la e alis, sulcus
Figu e 1. Schema ic ep esen a ion o he shu le box adap ed o ish condi ioning. A, Top
iew.B,Side iew.Thesys em o de ec ing he ish’spassingac oss heba ie consis edo wo
ed ligh s (24 V cc, 0.3 W) used as pho oemi e s, and a pai o pho o esis o s (3 V cc) used as
pho o ecep o s,allon heba ie .Theba ie wasmadeo g ayPVC.Todeli e heelec icshock
(ES) as an uncondi ioned s imulus (0.39 V/cm, 50 Hz), wo s ainless s eel ba s in con ac wi h
ou me alpla es we eused aselec odes.Two g eenligh s [disc imina i es imulus (DS)]we e
used as a condi ioned s imulus (10 W, 220 V AC, 50 Hz), which was p esen ed h ough he
anslucen end walls o he box.
2336 •J. Neu osci., Ma ch 3, 2004 •24(9):2335–2342 Po a ella e al. •In ol emen o he Fish Telencephalic Pallium in A oidance Lea ning
limi ans elencephali, and an e io commissu e we e used as ana omical
e e ences o de e mine he loca ion and ex en o he neu al issue o be
emo ed. A e he abla ion, he piece o skull was eplaced in i s o iginal
posi ion and ixed wi h cyanoc yla e glue. The ish was e u ned o i s
home ank o a eco e y pe iod o 5 d. Sham ope a ions we e pe o med
exac ly as desc ibed, excep ha he ne ous issue was no inju ed. The
con ol g oup did no ecei e any su gical in e en ion.
A he end o he expe imen , he ish wi h elencephalic lesions and
sham ope a ions we e deeply anes he ized (1:5000) and pe used wi h 50
mL o 0.9% saline solu ion, ollowed 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 ain was emo ed
om he skull, inspec ed o a p elimina y e alua ion o he abla ion, and
cu in ans e sal sec ions (50
␮
m hick) o his ological analysis.
Re en ion. A e he eco e y pe iod, he animals we e placed in he
shu le box, ollowing he same p ocedu e, o six addi ional sessions.
La ency and a oidance and escape esponses we e eco ded. The pe o -
mance du ing he sessions in he pos su gical pe iod was analyzed and
compa ed wi h he pos c i e ion sessions be o e su ge y o each g oup.
The eco ded a iables we e he same as in he p esu gical pe iod.
ANOVA wi h epea ed measu emen s was used o s a is ical analysis.
S a is ical pos hoc analysis was pe o med [hones ly signi ican di e -
ence (HSD)-Tukey es ]. S uden ’s es was used o compa e p esu gical
and pos su gical in ag oup di e ences.
Expe imen 2: ace wo-way ac i e a oidance condi ioning
Damage o he hippocampus in mammals p oduces a de ici in ace
condi ioning (Thompson e al., 1987; Moye e al., 1990). The aim o his
expe imen was o de e mine whe he a lesion o he la e al pallium o he
ish elencephalon could p oduce a de ici in ace a oidance condi ion-
ing compa able wi h ha p oduced by a hippocampal lesion in mam-
mals. To his end, he du a ion and empo al ela ion be ween he dis-
c imina i e s imulus (g een ligh ) and a e si e s imulus (elec ic shock)
we e modi ied. The s imuli we e no o e lapped; a gap o 5 sec be ween
g een ligh o and elec ic shock on was in oduced. The me hod pe -
o med he e had been success ully used in p e ious s udies in ish. Thus,
condi ioning o he emo ional esponse in elencephalon-abla ed ish
was ob ained wi h he same empo al in e s imulus in e al (O e mie
and Sa age, 1974); and he cue–shock onse in e al (15 sec) allows wo-
way a oidance condi ioning in ish (Da is, 1968; Sa age, 1969; Ze bolio
and Royal y, 1983; Po a ella e al., 2003).
Subjec s
Fi y expe imen ally nai e gold ish, om he same sou ce as and wi h
cha ac e is ics simila o hose o he animals o he p e ious expe imen ,
se ed as subjec s. The animals we e kep unde he same condi ions o
empe a u e, ligh /da k cycle, and ood desc ibed o Expe imen 1.
Appa a us
The expe imen al appa a us was he same as desc ibed o expe imen 1.
P ocedu e
P eexposu e. The p eexposu e p ocedu e was he same as ha used in he
p e ious expe imen .
Acquisi ion. All animals we e ained using he same p ocedu e. This
consis ed o a daily session o 10 ials sepa a ed by an ITI o a ying
du a ion, anging be ween 1 and 2 min. A he end o he ITI, he ial
began. The disc imina i e s imulus was u ned on o a maximum du a-
ion o 10 sec in he compa men whe e he ish was loca ed, ollowed by
a gap pe iod o 5 sec a e e mina ion o he disc imina i e s imulus.
Thus, he empo al sepa a ion be ween cue onse and shock onse was 15
sec. I he ish did no espond (swimming ac oss he ba ie ) wi hin 15
sec, he elec ic shock was u ned on o a maximum o 5 sec. A esponse
du ing he i s 15 sec inished he wa ning s imulus (g een ligh ), and he
shock was no deli e ed. A esponse du ing he 15–20 sec pe iod canceled
bo h he wa ning s imulus and he shock. Be o e s a ing and a e in-
ishing he daily aining session, he subjec es ed in he shu le box o 5
min wi hou any s imulus p esen a ion. The animals we e ained un il
hey eached he lea ning c i e ion, o a maximum o 30 sessions. The
lea ning c i e ion was he same as desc ibed abo e. The animals eached
he c i e ion be ween sessions 12 and 18 and we e andomly assigned o
one o i e g oups: MP abla ion (n⫽8), LP abla ion (n⫽8), TEL
abla ion (n⫽8), sham-ope a ed (n⫽8), and con ol (n⫽8). The
eco ded a iables we e la ency o esponses and pe cen age o a oidance
(shu le esponses occu ing be o e shock onse , when he la ency was
⬍15 sec) and escape (shu le esponses occu ing du ing shock, when he
la ency was be ween 15 and 20 sec). ANOVA wi h epea ed measu e-
men s was used o s a is ical analysis.
Su ge y. The su gical p ocedu e was he same
as o expe imen 1.
Re en ion. A e he eco e y pe iod, he ani-
mals we e placed in he shu le box, ollowing he
same p ocedu e, o six addi ional acquisi ion ses-
sions. La ency and a oidance and escape e-
sponses we e eco ded. The pe o mance du ing
he sessions in he pos su gical pe iod was ana-
lyzed and compa ed wi h ha o he pos c i e-
ion sessions be o e su ge y o each g oup. The
eco ded a iables we e he same as in he p esu -
gical pe iod. ANOVA wi h epea ed measu e-
men s was used o s a is ical analysis. S a is ical
pos hoc analysis was pe o med (HSD-Tukey
es ). S uden ’s es was used o compa e p esu -
gical and pos su gical in ag oup di e ences.
Resul s
Expe imen 1: wo-way ac i e
a oidance condi ioning
His ological analysis
A e isual and his ological inspec ion o he
b ain, one animal om each expe imen al
g oup showed in ac anial hemo hage, and
hei da a we e excluded om he analysis.
Thus, he g oups we e con ol (n⫽8),
sham-ope a ed (n⫽8), TEL abla ion
(n⫽7), MP lesion (n⫽7), and LP lesion
(n⫽7).
Figu e 2. Schema ic ep esen a ion o he loca ion and ex en o he lesions in expe imen 1: whole TEL, LP, and MP lesions.
Ligh shading ep esen s he la ges ex ension, and da k shading ep esen s he smalles . ac, An e io commissu e; N , nucleus
aenia. Pallium: Dd,A ea do salis elencephali pa s do salis. Subpallium: V, Ven al pallium; Vl, a ea en alis elencephali pa s
la e alis; V , a ea en alis elencephali pa s en alis. Fo o he abb e ia ions, see Resul s. The numbe s indica e he dis ance
(millime e s) om he os al pole o he elencephalon.
Po a ella e al. •In ol emen o he Fish Telencephalic Pallium in A oidance Lea ning J. Neu osci., Ma ch 3, 2004 •24(9):2335–2342 • 2337
Figu e 2 shows he la ges (pale shading) and he smalles
(da k shading) lesions o each expe imen al g oup. The bo de s
o each elencephalic a ea ollow he nomencla u e used else-
whe e (Pe e and Gill, 1975; Nieuwenhuys and Meek, 1990; Ro-
d ı´guez e al., 2002). The medial pallium lesions a ec ed he a ea
do salis elencephali pa s medialis en alis (Dm ) comple ely
and pa o he a ea do salis elencephali pa s medialis do salis
(Dmd). Colla e ally, in he mo e ex ensi e lesions, pa s o he
a ea elencephali pa s do salis cen alis (Dc), a ea elencephali
en alis pa s do salis (Vd), and a ea elencephali en alis pa s
pos -commissu alis (Vp) we e also a ec ed. La e al pallium le-
sions ex ended o he a ea do salis elencephali pa s la e alis en-
alis (Dl ) and he a ea do salis elencephali pa s la e alis do sa-
lis (Dld). Majo ex ension included small pa s o he Dc and a ea
do salis elencephali pa s do salis (Dd). The elencephalon-
abla ed animals showed comple e abla ion o he elencephalon,
and he his ological analysis showed no damage o he p eop ic
a ea and op ic ac s. The op ic ec um was also spa ed. None o
he sham-ope a ed animals exhibi ed any e idence o damage o
he elencephalon o op ic ec um.
Acquisi ion o condi ioned a oidance esponse
Once he animals eached he c i e ion o lea ning, he aining
and acquisi ion pe iod inished. A his ime, he la ency and
pe cen age o a oidance o he six sessions o c i e ion le el we e
analyzed and compa ed be ween he expe imen al g oups. An
ANOVA wi h epea ed measu emen s was used o s a is ical
analysis. The e we e no signi ican di e ences be ween he i e
g oups in ei he la ency (F
(4,32)
⫽1.975; p⬎0.19) o a oidance
(F
(4,32)
⫽1.256; p⬎0.3). Be o e su ge y, he a oidance and
la ency alues we e simila among all g oups in his phase (Fig. 3).
Re en ion o condi ioned a oidance esponse
The esul s o he e en ion pe iod, a e su ge y, showed s a is-
ically signi ican in e g oup di e ences in la ency (ANOVA wi h
epea ed measu emen s, F
(4,32)
⫽34.237; p⬍0.001) and a oid-
ance esponse (F
(4,32)
⫽18.894; p⬍0.001; Fig. 3A,B). Pos hoc
analyses p esen ed di e ences be ween he elencephalon-
abla ed g oup and he con ol, sham-ope a ed, and LP g oups in
a oidance (HSD-Tukey,
␣
⫽0.05; p⬍0.001) and la ency ( p⬍
0.001). The MP g oup showed simila di e ences wi h he h ee
named g oups (con ol, sham-ope a ed, and LP) in a oidance
and la ency ( p⬍0.001; Fig. 3A,B). In con as , he analyses om
he elencephalon-abla ed and MP g oups did no indica e any
di e ence in la ency ( p⫽1.0) o a oidance esponse ( p⬎0.91;
Fig. 3A,B). The e was no signi ican di e ence among con ol,
sham-ope a ed, and LP g oups in ei he a oidance esponse ( p⬎
0.74) o la ency ( p⬎0.51; Fig. 3A,B).
The compa ison be ween p esu gical (acquisi ion) and pos -
su gical ( e en ion) phases indica ed conside able impai men in
he e en ion o he p e iously acqui ed a oidance esponse, p o-
duced by whole elencephalon and medial abla ions (Fig. 3A).
The wo- ailed S uden ’s es (las session o acquisi ion s i s
session o e en ion) e ealed s a is ical di e ences in a oidance
in he elencephalon-abla ed g oup (
(6)
⬎19.4; p⬍0.001) and
MP g oup (
(6)
⬎17.6; p⬍0.001). The o he g oups did no show
any s a is ically signi ican di e ence in a oidance (con ol,
(7)
⬍
0.32; p⬎0.76; sham-ope a ed,
(7)
⬍1.35; p⬎0.21; and LP,
(6)
⬍1.018; p⬎0.34; Fig. 3A). The la ency o sham-ope a ed and
con ol g oups did no p esen any signi ican di e ence (
(7)
⬍
1.82; p⬎0.18;
(7)
⬍1.737; p⬎0.12, espec i ely); he LP g oup
p esen ed signi ican di e ences wi h he i s session o he e-
en ion phase (
(6)
⫽3.992; p⬍0.007) bu main ained a high
le el o a oidance esponse in he ollowing sessions; he
elencephalon-abla ed and MP g oups showed signi ican di e -
ences (
(6)
⬎6.59; p⬍0.001;
(6)
⬎7.64; p⬍0.001; Fig. 3B).
These esul s clea ly show ha he p e iously acqui ed condi-
ioned a oidance esponse was impai ed by medial pallium and
whole elencephalon abla ions (Fig. 3A,B). Al hough he da a o
la ency showed a p og essi e dec ease o he la ency alues in all
g oups (F
(5, 160)
⫽11.716; p⬍0.012) along he pos su gical e-
en ion pe iod (Fig. 3B), he la ency alues in he LP, sham-
ope a ed, and con ol g oups emained lowe han 10 sec (a oidance
la ency). In con as , la ency in he elencephalon-abla ed and MP
g oups la ency exceeded 10 sec (escape la encies; Fig. 3B).
Expe imen 2: ace wo-way ac i e a oidance condi ioning
His ological analysis
No ascula acciden s we e de ec ed by isual and his ological
inspec ion in any o he animals; hus, he expe imen al g oups
we e con ol (n⫽8), sham-ope a ed (n⫽8), TEL abla ion (n⫽
8), MP lesion (n⫽8), and LP lesion (n⫽8).
Figu e 4 shows he ex en o he lesions in he expe imen al
g oups. The la ges (pale shading) and smalles (da k shading)
medial and la e al pallium lesions we e econs uc ed on s an-
da d co onal sec ions o he same gold ish a las. The medial pal-
lium lesions a ec ed he Dm a ea almos comple ely and he
Dmd a ea pa ially, wi h mino damage o adjacen a eas. Colla -
e ally, in he mo e ex ensi e lesions, po ions o he Dc, Vd, Vp,
Figu e 3. Non ace a oidance condi ioning pe o mance o he di e en g oups du ing he
acquisi ion and e en ion phases in expe imen 1. A, Mean ⫾SEM o pe cen age o a oidance
esponse du ing acquisi ion (6 sessions a e eaching lea ning c i e ion be o e su ge y) and
e en ion (6 sessions a e su ge y) phases. B, Mean ⫾SEM o esponse la ency (seconds)
du ing acquisi ion and e en ion pe iods.
2338 •J. Neu osci., Ma ch 3, 2004 •24(9):2335–2342 Po a ella e al. •In ol emen o he Fish Telencephalic Pallium in A oidance Lea ning
and a ea en alis elencephali pa s sup acommissu alis (Vs)
we e also a ec ed. La e al pallium lesions included he Dl and
Dld, and he majo ex ension lesions included small pa s o he
Dc and Dd. The elencephalon abla ions we e comple e and did
no a ec he p eop ic a ea, op ic ac s, o op ic ec um. The
sham-ope a ed animals did no p esen any damage in he elen-
cephalon o op ic ec um.
Acquisi ion o condi ioned a oidance esponse
As in he p e ious expe imen , he aining and he acquisi ion
pe iod inished when he animals eached he c i e ion o lea n-
ing. The la ency and a oidance o he acquisi ion c i e ion le el
sessions we e compa ed and analyzed be ween he expe imen al
g oups. The ANOVA analysis wi h epea ed measu emen s
showed no signi ican di e ences be ween he i e g oups in ei-
he la ency (F
(4, 33)
⫽2.3; p⬎0.08) o a oidance (F
(4, 33)
⫽
0.833; p⬎0.51; Fig. 3A,B). Be o e su ge y, he a oidance e-
sponse and he la ency alues we e simila in all g oups (Fig. 5).
Re en ion o condi ioned a oidance esponse
In his phase, s a is ically signi ican di e ences be ween he ex-
pe imen al g oups in a oidance esponse (ANOVA wi h epea ed
measu emen s; F
(4, 33)
⫽21.742; p⬍0.001) and la ency (F
(4, 33)
⫽
16.58; p⬍0.001) we e ound (Fig. 4A,B). Pos hoc analyses indi-
ca ed signi ican di e ences be ween he elencephalon-abla ed,
sham-ope a ed, and con ol g oups in a oidance (HSD-Tukey,
␣
⫽0.05; p⬍0.001) and la ency ( p⬍0.001; Fig. 5A,B). The MP
g oup showed signi ican di e ences wi h he sham-ope a ed and
con ol g oups in a oidance and la ency ( p⬍0.001; Fig. 5A,B).
In e es ingly, in his expe imen , he LP g oup also p esen ed
s a is ically signi ican di e ences wi h he sham-ope a ed and
con ol g oups in a oidance ( p⬍0.001) and la ency ( p⬍0.001;
Fig. 5A,B). The sham-ope a ed and con ol g oups did no
p esen signi ican di e ences in ei he a oidance ( p⬎0.95) o
la ency ( p⬎0.98). Finally, he pe o mance o he h ee b ain-
inju ed expe imen al g oups was simila in a oidance ( p⬎0.83)
and la ency ( p⬎0.61; Fig. 5).
The acquisi ion and he e en ion
phase we e compa ed by means o a wo-
ailed S uden ’s es (las session o acqui-
si ion s i s session o e en ion). Resul s
indica ed signi ican di e ences o he
elencephalon-abla ed, MP, and LP
g oups in a oidance (
(7)
⬎7.04; p⬍
0.001;
(6)
⬎11.310; p⬍0.001;
(7)
⬎
10.247; p⬍0.001, espec i ely) and la-
ency (
(7)
⬎4.959; p⬍0.002;
(6)
⬎6.55;
p⬍0.001;
(7)
⬎13.69; p⬍0.001, espec-
i ely; Fig. 5A,B). The sham-ope a ed and
con ol g oups did no p esen any di e -
ences in ei he a oidance (
(7)
⬍2.03; p⬎
0.82;
(6)
⬍1.68; p⬎0.14, espec i ely) o
la ency (
(7)
⬍1.452; p⬎0.19;
(6)
⬍1.733;
p⬎0.13, espec i ely; Fig. 5A,B). Thus,
he esul s o expe imen 2 showed ha
when he expe imen al p ocedu e empha-
sized he empo al ac o , he LP lesion
p oduced de as a ing de ici s in condi-
ioned a oidance lea ning (Figs. 3, 5).
Discussion
In ol emen o he gold ish medial
pallium in a oidance condi ioning
The p esen esul s show, o he i s ime,
ha damage o he eleos ish medial pal-
lium p oduces a de ici in he e en ion o condi ioned a oidance
as se e e as ha a e abla ion o he whole elencephalon (Sa -
age, 1969; O e mie and Papini, 1985, 1986; Papini, 1985; O e -
mie and Hollis, 1990). In con as , he la e al pallium lesion had
no signi ican e ec s on he e en ion o a oidance in he non-
ace p ocedu e. The e o e, he p esen esul s sugges ha he
medial pallium could be he main elencephalic a ea in ol ed in
his kind o lea ning.
Al hough he la ency alues dec eased p og essi ely in he
elencephalon-abla ed and MP-lesioned g oups along he pos -
su gical aining sessions in he non ace p ocedu e (expe imen
1), la ency was consis en ly ⬎10 sec (escape la ency) wi hou
eaching a oidance alues du ing he e en ion pe iod (Fig. 3).
These da a indica e ha he elencephalon-abla ed and MP-
lesioned animals we e able o imp o e escape esponses along he
pos su gical sessions bu no o p oduce a oidance esponses. In
a p e ious s udy (Sa age, 1969), o eb ain-less ish eached, a e
su ge y, a oidance esponse le els simila o hose o he MP
g oup in he p esen expe imen (⬃50%), bu hey did no exceed
his pe cen age along 26 sessions.
The e is good e idence ha a oidance lea ning is based on he
acquisi ion o a media ional s a e o ea in gold ish (Gallon,
1972; O e mie and S a kman, 1974; Po a ella e al., 2003),
which, in u n, con ibu es o he de elopmen o he ins umen-
al a oidance s imulus– esponse associa ion because o a educ-
ion in ea a e he shu le esponse (Mow e , 1960; Flood e al.,
1976; O e mie and Hollis, 1990; Zhuiko e al., 1994; Po a ella
e al., 2003). The de ici caused by he MP lesion in gold ish could
be a ibu able o a de ici in he e ie al o he an icipa o y ea
esponse o he wa ning s imulus o could be caused by in e e -
ing wi h he abili y o an in e nal s a e o ea o induce an a oid-
ance esponse (Mow e , 1960; Flood e al., 1976). Thus, he
p esen esul s indica e ha he ish elencephalon con ains an
emo ional sys em ha is c i ical o ea condi ioning, and he
MP is an essen ial elemen in his specialized sys em. The MP o
Figu e 4. Schema ic ep esen a ion o he loca ion and ex en o he lesions in expe imen 2: whole TEL, LP, and MP lesions.
Ligh shading ep esen s he la ges ex ension, and da k shading ep esen s he smalles . Fo abb e ia ions, see Resul s and
Figu e 2 legend.
Po a ella e al. •In ol emen o he Fish Telencephalic Pallium in A oidance Lea ning J. Neu osci., Ma ch 3, 2004 •24(9):2335–2342 • 2339

eleos ish has been p oposed as ana omically homologous o he
pallial amygdala o mammals (Nieuwenhuys and Meek, 1990;
B a o d, 1995; No hcu , 1995; Bu le 2000). In consonance wi h
his p oposal, he p esen esul s demons a e a s iking unc-
ional simila i y be ween he eleos MP and he pallial amygdala
(Aggle on, 1992, 2001; LeDoux, 1995). In con as , an MP lesion
does no impai lea ned mo o esponses (as indica ed by he low
escape la encies o he animals in he MP-lesioned g oup), spa ial
memo y (Rod ı´guez e al., 2002), o ace a oidance lea ning
(p esen esul s, expe imen 2). Thus, he p esen esul s do no
suppo he p oposal o homology be ween he eleos ish MP
(Dm ) and he land e eb a e basal ganglia o he hippocampus
(Ech ele and Saidel, 1981; Mu akami e al., 1983; I o e al., 1986;
Pa en , 1986) on he basis o unc ional ea u es.
In ol emen o he gold ish la e al pallium in ace
a oidance condi ioning
Unlike in expe imen 1, he LP lesion impai ed pe o mance in
he ace-condi ioning p ocedu e. The main di e ence be ween
he beha io al p ocedu es used in expe imen s 1 and 2 was he
p esence o an in e s imulus empo al gap o 5 sec ( ace a oid-
ance condi ioning). Consequen ly, ou esul s show ha he LP
o ac inop e ygian ish plays a majo ole in he e en ion o con-
di ioned a oidance in a ace p ocedu e. The la e al pallium o
eleos ish, like he hippocampus o mammals, is in ol ed in he
analysis o empo al a ibu es o he ask, he main enance o he
ace o he wa ning s imulus o condi ioning, o bo h. The
mammalian hippocampus seems o be in ol ed in he acquisi-
ion and e en ion o condi ioned a oidance, condi ioned ea ,
and ace condi ioning when con ex ual, spa ial, and empo al
ac o s a e ele an o es ablishing associa ions be ween s imuli
and esponses (O’Kee e and Nadel, 1978; Wood u and Kan o ,
1983; Meck e al., 1984; Ol on, 1986; Kesne and DiMa ia, 1987;
Thompson e al., 1987; Moye e al., 1990; Phillips and LeDoux,
1992; Rawlins e al., 1993; Yee and Rawlins, 1994; Cassaday and
Rawlins, 1995; Co odimas and LeDoux, 1995; Winocu , 1997).
Mo e speci ically, i has been p oposed ha he mammalian hip-
pocampus is di ec ly in ol ed in he p ocessing o he du a ion,
sequence, and empo al o de o s imuli (Meck e al., 1984; Ol-
on, 1986; Kesne and DiMa ia, 1987). The p esen esul s hus
demons a e a s iking unc ional simila i y be ween he mam-
malian hippocampal pallium and he LP o eleos ish and sup-
po he hypo hesis o homology be ween he ish LP and he
mammalian hippocampus p e iously p oposed on he basis o
mo phological ea u es (Nieuwenhuys and Meek, 1990; B a o d,
1995; No hcu , 1995; Bu le , 2000) and unc ional da a (Rod ı´-
guez e al., 2002).
Howe e , he hippocampus has no been ela ed o empo al
p ocessing unc ions in nonmammalian e eb a es (Macphail,
1987, 1996; Bingman, 1990; Hamp on and She lewo h, 1996;
Macphail, 1987, 1996). Fu he mo e, some au ho s ha e p o-
posed ha he nonspa ial unc ions o he mammalian hip-
pocampus may be ela ed o unsough damage o co ical a eas
adjacen o he hippocampus (e.g., en o hinal co ex) du ing he
su gical p ocedu e (O’Kee e, 1993; Nadel, 1995; Guillazo-Blanch
e al., 2002). Thus, hese co ical a eas (close o he hippocampus)
may be in ol ed in nonspa ial unc ions (i.e., empo al a ibu e
p ocessing). In ou case, he lesions o he LP ex ended o he Dld,
which has been p oposed as homologous o he isoco ex o e -
apods (B a o d and No hcu , 1974; No hcu and B a o d,
1980; No hcu and Da is, 1983; Bu le , 1994). Al hough u he
s udies on he unc ional implica ions o he ish la e al pallium
a e necessa y, ou esul s p esen a hough -p o oking scene in
which he unc ional in ol emen o he eleos ish LP is dis-
cussed in unc ional and heo e ical e ms simila o hose o
hippocampal o ma ion.
Teleos ish medial and la e al elencephalic pallia main ain
unc ional pa allelism wi h mammalian hippocampus and
amygdala: implica ions o e eb a e o eb ain e olu ion
The p esen esul s demons a e a s iking unc ional simila i y
be ween he MP and LP o eleos ish and he pallial amygdala
and hippocampal pallium o mammals, espec i ely. On he basis
o ana omical and de elopmen al e idence, he MP o eleos ish
is conside ed homologous o he pallial amygdala o mammals,
whe eas he LP co esponds o he hippocampal pallium (No h-
cu and B a o d, 1980; Nieuwenhuys and Meek, 1990; B a o d,
1995; Bu le , 2000). The o eb ain o ay- inned ishes de elops
by a p ocess o e e sion o ou wa d bending o he p osence-
phalic walls o he p osencephalic esicle (Nieuwenhuys, 1963;
No hcu and B a o d, 1980). This e e sion p ocess e e ses he
pallial o medial- o-la e al opog aphy obse ed in mammals.
Thus, he de elopmen ally la e al (amygdala ) pallium is p e-
dic ed as lying medially in ay- inned ishes, whe eas he de el-
opmen ally la e al (hippocampal) pallium is p edic ed as occu-
pying a medial posi ion. The p esen unc ional da a p o ide
addi ional suppo o he e e sion hypo hesis o eleos elen-
cephalon de elopmen , wi h conside able p ese a ion o he
Figu e5. T ace a oidance condi ioning pe o manceo he di e en g oups du ingacquisi-
ionand e en ionphasesinexpe imen 2.A,Mean⫾SEMo pe cen ageo a oidance esponse
in acquisi ion (6 sessions a e eaching he lea ning c i e ion be o e su ge y) and e en ion (6
sessionsa e su ge y)phases. B,Mean⫾SEM o esponsela ency (seconds)inacquisi ionand
e en ion pe iods.
2340 •J. Neu osci., Ma ch 3, 2004 •24(9):2335–2342 Po a ella e al. •In ol emen o he Fish Telencephalic Pallium in A oidance Lea ning
o iginal opology, and could con ibu e signi ican ly o cla i ying
he iden i y o he pallial a eas in ay- inned ishes.
Fu he mo e, he close simila i y be ween he unc ion o ho-
mologous elencephalic pallial a eas sugges s ha he o eb ain o
e eb a es con ains a common, conse ed pa e n o basic o ga-
niza ion. Ray- inned ishes and land e eb a es sha e a common
ances o ha li ed some 400 million yea s ago (Ca oll, 1988).
Following a pa simony p inciple, he p esen esul s sugges ha
a sys em o emo ional memo y (medial pallium based) and an-
o he (o o he s) o spa ial, ela ional, o empo al memo y (la -
e al pallium based) could ha e appea ed ea ly du ing phylogen-
esis and could ha e been conse ed h oughou e eb a e
e olu ion.
Re e ences
Aggle on JP (1992) The amygdala: neu obiological aspec s o emo ion,
memo y, and men al dys unc ion. New Yo k: Wiley-Liss.
Aggle on JP (2001) The amygdala: a unc ional analysis. Ox o d: Ox o d
UP.
Amb ogi-Lo enzini C, Buche elli C, Giache i A, Mugnai L, Tassoni G
(1991) E ec s o nucleus basola e alis amygdalae neu o oxic lesions on
a e si e condi ioning in he a . Physiol Beha 49:765–770.
Bingman VP (1990) Spa ial na iga ion in bi ds. In: Neu obiology o com-
pa a i e cogni ion (Kesne R, Ol on DS, eds), pp 423–447. Hillsdale, NJ:
E lbaum.
B a o d MR (1995) Compa a i e aspec s o o eb ain o ganiza ion in he
ay- inned ishes: ouchs ones o no ? B ain Beha E ol 46:259–274.
B a o d MR, No hcu GR (1974) Ol ac o y bulb p ojec ions in he bichi ,
Polyp e us. J Comp Neu ol 156:165–178.
Bu le AB (1994) The e olu ion o he do sal pallium in he elencephalon o
amnio es: cladis ic analysis and a new hypo hesis. B ain Res Re
19:66–101.
Bu le AB (2000) Topog aphy and opology o he eleos elencephalon: a
pa adox esol ed. Neu osci Le 293:95–98.
Ca oll RL (1988) Ve eb a e paleon ology and e olu ion. New Yo k:
F eeman.
Cassaday HJ, Rawlins JNP (1995) Fo nix- imb ia sec ion and wo king
memo y de ici s in a s: s imulus complexi y and s imulus size. Beha
Neu osci 109:594–606.
Co odimas KP, LeDoux JE (1995) Dis up i e e ec s o pos aining pe i hi-
nal co ex lesions on condi ioned ea : con ibu ions o con ex ual cues.
Beha Neu osci 109:613–619.
Da is RE (1968) En i onmen al con ol o memo y ixa ion in gold ish.
J Comp Physiol Psychol 65:72–78.
Ech ele SM, Saidel WM (1981) Fo eb ain p ojec ions in he gold ish sup-
po elencephalic homologies wi h land e eb a es. Science
212:683–685.
Eichenbaum H, O o T, Cohen NJ (1992) The hippocampus: wha does i
do? Beha Neu al Biol 57:2–36.
Flood NB, O e mie JB, Sa age GE (1976) The eleos elencephalon and
lea ning: an in e p e a i e e iew o da a and hypo heses. Physiol Beha
16:783–798.
Gallon RL (1972) E ec s o p e- aining wi h ea and escape condi ioning
on shu le-box a oidance acquisi ion by gold ish. Psychol Rep
31:919–924.
G ay JA, McNaugh on N (1983) Compa ison be ween he beha iou al e -
ec s o sep al and hippocampal lesions: a e iew. Neu osci Biobeha Re
7:119–188.
G ossman SP, G ossman L, Walsh L (1975) Func ional o ganiza ion o he
a amygdala wi h espec o a oidance beha io . J Comp Physiol Psychol
88:829–850.
Guillazo-Blanch G, Nadal R, Vale-Ma inez A, Ma ı´-Nicolo ius M, A e´ alo
R, Mo gado-Be nal I (2002) E ec s o imb ia lesions on ace wo-way
ac i e a oidance acquisi ion and e en ion in a s. Neu obiol Lea n Mem
78:406–425.
Hamp on RR, She lewo h S (1996) Hippocampal lesions impai memo y
o loca ion bu no colo in passe ine bi ds. Beha Neu osci
110:831–835.
Ho ne JL, Longo N, Bi e man ME (1961) A shu le box o ish and a
con ol ci cui o gene al applicabili y. Am J Psychol 74:114–120.
I o H, Mu akami T, Fukuoka T, Kishida R (1986) Thalamic ibe connec-
ions in a eleos (Sebas icus ma mo a us): isual, soma osenso y, oc a ol-
a e al, and ce ebella elay egion o he elencephalon. J Comp Neu ol
250:215–227.
Kesne RP, DiMa ia BV (1987) Neu obiology o an a ibu e model o
memo y. P og Psychobiol Physiol Psychol 12:207–277.
LeDoux JE (1995) Emo ions: clues om he b ain. Annu Re Psychol
46:209–235.
Macphail EM (1987) B ain and in elligence in e eb a es. Ox o d:
Cla endon.
Macphail EM (1996) Cogni i e unc ion in mammals: he e olu iona y pe -
spec i e. Cogni B ain Res 3:279–290.
Ma ino-Ne o J, Sabba ini RM (1983) Disc e e elencephalic lesions accele -
a e he habi ua ion a e o beha io al a ousal esponses in Siamese igh -
ing ish (Be a splendens). B az J Med Biol Res 16:271–278.
McIn y e M, S ein DG (1973) Di e en ial e ec s o one- e sus wo-s age
amygdaloid lesions on ac i i y, explo a ion, and a oidance beha io in
he albino a . Beha Biol 9:451–465.
Meck WH, Chu ch RM, Ol on DS (1984) Hippocampus, ime and memo y.
Beha Neu osci 98:3–22.
Mow e OH (1960) Lea ning heo y and beha io . New Yo k, Wiley.
Moye J JR, Deyo RA, Dis e ho JE (1990) Hippocampec omy dis up s
ace eye-blink condi ioning in abbi s. Beha Neu osci 104:243–252.
Mu akami T, Mo i a Y, I o H (1983) Ex insic and in insic ibe connec-
ions o he elencephalon in a eleos , Sebas icus ma mo a us. J Comp
Neu ol 216:115–131.
Nadel L (1995) The ole o he hippocampus in decla a i e memo y: a com-
men on Zola-Mo gan, Squi e, and Ramus (1994). Hippocampus
5:232–239.
Nieuwenhuys R (1963) The compa a i e ana omy o he ac inop e igian
o eb ain. J Hi n o sch 6:171–200.
Nieuwenhuys R, Meek J (1990) The elencephalon o ac inop e ygian ishes.
In: Compa a i e s uc u e and e olu ion o he ce eb al co ex (Jones EG,
Pe e s A, eds), pp 31–73 New Yo k: Plenum.
No hcu RG (1995) The o eb ain o gna hos omes: in sea ch o a mo -
pho ype. B ain Beha E ol 46:275–318.
No hcu RG, B a o d MR (1980) New obse a ions on he o ganiza ion
and e olu ion o he elencephalon o ac inop e ygian ishes. In: Compa -
a i e neu ology o he elencephalon (Ebbesson SOE, ed), pp 41–98. New
Yo k: Plenum.
No hcu RG, Da is RE (1983) Telencephalic o ganiza ion in ay- inned
ishes. In: Fish neu obiology, Vol 2 (No hcu RG, Da is RE, eds), pp
203–236. Ann A bo : Uni e si y o Michigan.
O’Kee e J (1993) Hippocampus, he a, and spa ial memo y. Cu Opin
Neu obiol 3:917–924.
O’Kee e J, Nadel L (1978) The hippocampus as a cogni i e map. Ox o d:
Cla endon.
Ol on DS (1986) Hippocampal unc ion and memo y o empo al con ex .
In: The hippocampus, Vol 3 (Isaacson RL, P ib am KH, eds), pp 281–298.
New Yo k: Plenum.
O e mie JB, Hollis KL (1990) Fish in he hink ank: lea ning, memo y and
in eg a ed beha io . In: Neu obiology o compa a i e cogni ion (Kesne
RP, Ol on DS, eds), pp 204–236. Hillsdale, NJ: E lbaum.
O e mie JB, Papini MR (1985) Se ial abla ions o he elencephalon and
a oidance lea ning by gold ish (Ca assius au a us). Beha Neu osci
99:509–520.
O e mie JB, Papini MR (1986) Fac o s modula ing he e ec s o eleos
elencephalon abla ion on e en ion, elea ning, and ex inc ion o ins u-
men al a oidance beha io . Beha Neu osci 100:190–199.
O e mie JB, Sa age GE (1974) E ec s o elencephalic abla ion on ace
classical condi ioning o hea a e in gold ish. Exp Neu ol 42:339–346.
O e mie JB, S a kman N (1974) T ans e o con ol o a oidance beha io
in no mal and elencephalon abla ed gold ish (Ca assius au a us). Physiol
Beha 12:605–608.
Papini MR (1985) A oidance lea ning a e simul aneous e sus se ial el-
encephalic abla ions in he gold ish. Bull Psychon Soc 23:160–163.
Pa en A (1986) Compa a i e neu obiology o he basal ganglia. New Yo k:
Wiley.
Pe e RE, Gill VE (1975) A s e eo axic a las and echnique o o eb ain
nuclei o he gold ish, Ca assius au a us. J Comp Neu ol 159:69–102.
Phillips RG, LeDoux JE (1992) Di e en ial con ibu ion o amygdala and
Po a ella e al. •In ol emen o he Fish Telencephalic Pallium in A oidance Lea ning J. Neu osci., Ma ch 3, 2004 •24(9):2335–2342 • 2341
hippocampus o cued and con ex ual ea condi ioning. Beha Neu osci
106:274–285.
Po a ella M, Va gas JP, Salas C, Papini MR (2003) In ol emen o he
elencephalon in spaced- ial a oidance lea ning in he gold ish (Ca as-
sius au a us). Physiol Beha 80:49–56.
Rawlins JNP, Ly o d GL, Se e iades A, Deacon RMJ, Cassaday HJ (1993)
C i ical de e minan s o non-spa ial wo king memo y de ici s in a s wi h
con en ional lesions o he hippocampus o o nix. Beha Neu osci
107:236–249.
Rod ı´guez R, Lo´pez JC, Va gas JP, Go´mez Y, B oglio C, Salas C (2002) Con-
se a ion o spa ial memo y unc ion in he pallial o eb ain o ep iles
and ay- inned ishes. J Neu osci 22:2894–2903.
Sa´nchez-Riolobos A (1986) Di e en ial e ec o chemical lesion and elec-
ocoagula ion o he cen al amygdaloid nucleus on ac i e a oidance
esponses. Physiol Beha 36:441–444.
Sa a SJ, Da id-Remacle M (1981) Disc imina i e a oidance lea ning in hip-
pocampal and co ical a s: acquisi ion a e, beha io al s a egies, and
long e m e en ion. Physiol Psychol 9:37–48.
Sa age GE (1969) Telencephalic lesions and a oidance beha io in he gold-
ish (Ca assius au a us). Anim Beha 17:362–373.
Schac e DL, Tul ing E (1994) Memo y sys em. Camb idge, MA: MIT.
Squi e LR (1992) Memo y and he hippocampus: a syn hesis om indings
wi h a s, monkeys, and humans. Psychol Re 99:195–231.
Thompson RF, Donegan NH, Nelson H, Cla k GA, La ond DG, Da id G,
Lincoln JS, Madden IV J, Manounas LA, Lau a A, Mauk MD, McCo mick
DA, Da id A (1987) Classical condi ioning, Chap 14 (Go mezano I,
P okasy WF, eds), pp 371–399. Hillsdale, NJ: E lbaum.
Va gas JP, Rod ı´guez F, Lo´pez JC, A ias JL, Salas C (2000) Spa ial lea ning-
induced inc ease in he a gy ophilic nucleola o ganize egion o do so-
la e al elencephalic neu ons in gold ish. B ain Res 865:77–84.
Weine I, Feldon J, Ta asch R, Hai s on I, Joel D (1998) Fimb ia- o nix cu
a ec s spon aneous ac i i y, wo-way a oidance and delayed non ma ch-
ing o sample, bu no la en inhibi ion. Beha B ain Res 96:59–70.
Winocu G (1997) Hippocampal lesions al e condi ioning o condi ional
and con ex ual s imuli. Beha B ain Res 88:219–229.
Wood u ML, Kan o H (1983) Fo nix lesions, plasma ACTH le els, and
shu le box a oidance in a s. Beha Neu osci 97:897–907.
Yee BK, Rawlins JNP (1994) The e ec s o hippocampal o ma ion abla ion
o imb ia- o nix sec ion on pe o mance o a non-spa ial adial a m
maze ask by a s. J Neu osci 14:3766–3774.
Ze bolio DJ, Royal y JL (1983) Ma ching and oddi y condi ional disc imi-
na ion in he gold ish as a oidance esponses: e idence o concep ual
a oidance lea ning. Anim Lea n Beha 11:341–348.
Zhuiko AY, Cou illon PA, Bi e man ME (1994) Quan i a i e wo-p ocess
analysis o a oidance condi ioning in gold ish. J Exp Psychol Anim Beha
P ocess 20:32–43.
2342 •J. Neu osci., Ma ch 3, 2004 •24(9):2335–2342 Po a ella e al. •In ol emen o he Fish Telencephalic Pallium in A oidance Lea ning