Effect of telencephalic ablation on appetitive instrumental learning in the goldfish (Carassius auratus)

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. R e e e n c e s Amsel, A. (1992). F us a ion heo y. Camb idge: Camb idge Uni e si y P ess. Boi ano, J. J.; Foske , M. D. (1968). E ec s o pa ial ein o cemen on speed o app oach esponses in gold ish (Ca assius au a us). Psycho - logical Repo s,22, 741-744. G ay, J. (1987). The psychology o ea and s ess.Camb idge: Camb idge Uni e si y P ess. Heinswo h, F. R.; O e mie , J. B.; Snowdon, C. T. (1967). Speci ic and pe manen de ici s in ins umen al a oidance esponding ollowing o- eb ain abla ion in he gold ish. Jou nal o Compa a i e and Physiolo - gical Psychology. 63, 111-116. Howell, D. C. (1992). S a is ical me hods o psychology. Thi d Edi ion. Bos on: PWS-Ken . EMILIO DURÁN, JUAN P. VARGAS, COSME SALAS AND MAURICIO R. PAPINI 524 Ja a d, L. E.; Isaacson, R. L. 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