II. Key stimuli in avoidance learning

Transcription

1 Anmal Learnng & Behavor 1986, 14 (/), Ethologcal analyss of predator avodance by the paradse fsh (Macropodus operculars L.): II. Key stmul n avodance learnng V. CSANYI L. Eotvos Unversty of Budapest. Hungary The possble role of eyespot patterns n predator recognton by paradse fsh was examned usng a passve avodance condtonng technque wth varous dummes or lve goldfsh. It was found that a low-ntensty shock, although clearly uncomfortable, elcted exploratory behavor n the fsh and that observable learnng dd not occur. However, fthe paradse fsh was shocked n the presence of a lve goldfsh or varous fsh dummes, exploraton dmnshed and avodance learnng was detected. Ths was characterzed by a consderable ncrease n latency to enter the shocked compartment. The most effectve dummes were those wth two laterally arranged eyelke spots. The possble role of speces-specfc key stmul n avodance learnng and organzng defensve behavor of the paradse fsh s dscussed. In a prevous study on predator recognton n paradse fsh (Csany, 1985), t was found that lve fsh from another speces, whether predatory or harmless n nature, elct vgorous approach behavor on the part of the paradse fsh. Repeated encounters wth the same speces lead to habtuaton. If the frst encounter resulted n an attack by the predator, the paradse fsh fled mmedately and n subsequent meetngs wth the same predator they demonstrated "avodance" behavor ndependently of the actons of the predator. Avodance behavor was also elcted by the harmless goldfsh f the paradse fsh had prevously been gven a mld electrc shock n the presence of the goldfsh. It was concluded that predator recognton was acheved by the paradse fsh through a learnng process that was based upon fear elctaton n the presence of fsh of another speces. Ths fndng s n agreement wth observatons of other prey anmals whch usually respond to a lve or model predator by approach and mobbng or by varous types of avodance behavor (Coss, 1978a, 1978b; Hnde, 1954; Kruuk, 1964). Although, n most cases, predator recognton has been found not to requre experence (Hrsch & Bolles, 1980), the role for learnng has also been shown (Curo, Ernst, & Veth, 1978; Kruuk, 1976). In the present studes, I wanted to nvestgate the characterstc features of predators that elct approach and, upon attack, flght. Qute plausble features to be consdered were the eyes, snce eyespot patterns have been well establshed as fearelctng stmul n a wde range of prey anmals, namely The author s very grateful to P. 1. B. Slater for hs valuable comments on earler drafts of ths manuscrpt. Thanks are also extended to Gy. Kamps for hs help n the statstcal analyss. The author's malng address s: Department of Behavor Genetcs. L. Eotvos Unversty of Budapest, Javorka S. u. 14. God, H-2131 Hungary. n brds (Blest, 1957; Jones, 1980), mammals (Coss, 1978a), and fsh (Coss, 1979). To examne the possble role of eyespot patterns n predator recognton by the paradse fsh, we used varous dummes and lve goldfsh. We chose a typcal passve avodance condtonng stuaton to test the effects of predatory features. Ths technque allowed for exact control of the expermental parameters. GENERAL METHODS Subjects The subjects were 528 female Macropodus operculars, F I hybrds of two nbred strans desgnated as strans Sand U. These fsh were bred n our laboratory. All the fsh were between 120 and 180 days old at the tme of the experment and were housed n ndvdual 30 x 15 x 15 ern aquara. The aquara were well fltered, temperature (28 0 C) was held constant, and each unt contaned one pece of water plant (Hygrophla polysperma). The anmals were fed daly on Tubfex worms. Apparatus Two dentcal40x20x20 ern shuttle-tanks were used (Fgure 1). The tanks were separated nto two compartments by a green plastc wall. whch contaned a 3-cm-dam crcular gate n the mddle. The nner walls ofthe dark compartment were covered wth a mxture of fne-gran sand and slcon rubber. Two stanless steel grds covered the whole walls of the two parallel sdes. Ths compartment was covered by a black-panted ld. The bottom of the lght compartment was also covered wth slcon and sand, but the sde walls were transparent. The lghtng n the apparatus was measured at 30 and 200 Ix n the dark and the lght sdes, respectvely. Shuttlng actvty was montored by an nfrared photoelectrc devce located n the gate. Ths devce also served as a trgger for a tran ofelectrc shock pulses f the fsh entered the dark compartment (20-msec trans of 500 Hz ac, 50- to loo-rna shocks every.2 sec, wth the frst tran beng gven mmedately after the fsh entered the compartment. When the fsh moved out of the dark compartment, the shocks ceased automatcaliy. The parameters of the shuttlng actvty, such as the latency of the frst crossng through the gate-that s, the tme from entry nto the tank to entry through 101 Copyrght 1986 Psychonomc Socety, Inc.

2 102 CSANYI I. elec trods -20cm-- I3cm Fgure 1. Shuttle-tank used n the passve avodance experments. the gate-nto the dark sde, the number of crossngs and the total amount of tme spent n the dark compartment durng a IS-mn tral were recorded automatcally. After every 5 anmals were tested, the water was replaced n the shuttle-tank. Both tanks were placed nto a loox loox 100 em deep enclosure that was covered by green plastc on fve sdes. Through the open sde of the enclosure, the movement of the fsh could be observed by the expermenter sttng behnd a green plastc screen. The enclosure was llumnated by sx whte fluorescent tubes (20 W) from above. Procedure Forty-eght hours pror to tranng, all the fsh were placed n ndvdual aquara. Durng the tranng sessons, whch were conducted twce a day, each fsh was placed, usng a small hand-net, nto the transparent compartment of the shuttle-tank, where t receved varous treatments. Ffteen mnutes later, the fsh was removed from the apparatus and returned to ts home tank. All tranng experments were carred out between 9:00 a.m. and 4:00 p.m. On the frst tral, some fsh (about 10%) dd not enter the dark compartment durng the IS mn allowed. In these cases, a small net was used to gently compel the fsh to swm through the gate; after I mn, the fsh was removed from the apparatus. Three dfferent tranng experments were carred out. In each experment, the frst four trals were allowed for habtuaton, durng whch nether an electc shock nor manpulatons wth varous dummes were appled. Further procedures are gven n the descrptons of the experments. In the statstcal analyss, the latency assgned to fsh that remaned n the transparent compartment durng the whole tral was 900 sec. EXPERIMENT 1 Method Eghty fsh were dvded nto four equal groups. Three of these groups were traned to avod the dark compartment by beng shocked from Tral S onward whenever they entered the dark. The shock ntenstes were 50, 75, and 100 rna. The fourth group served as a no-shock control. Results The effect of habtuaton durng Trals 1-4 was analyzed by a two-way ANOVA wth repeated measures (treatment x trals). There was a marked reducton of latency n subsequent trals [F(3,76) = 61.0, p <.001]. The amount oftme spent n the dark ncreased consderably durng habtuaton [F(3,76) = 106.9, P <.001]. The number of crossngs also ncreased sgnfcantly [F(3,76) = 28.8, P <.001]. There were no sgnfcant dfferences among the groups n treatments [F(3,76) = 1.1, F(3,76) = 0.87, F(3,76) = 1.05, for latency, tme spent n the dark, and number ofcrossngs, respectvely] or nteractons [F(9,228) = 0.47, F(9,228) = 1.51, F(9,228) = 0.74, for latency, tme spent n the dark, and for the number of crossngs, respectvely]. Therefore, the data of the varous groups on Trals 1-4 were combned n Fgures 2-4. Punshment by shock reversed the drecton of changes n all three parameters. Durng the shock trals (Trals 5-8, Fgures 2, 3, and 4), latency ncreased and the tme spent n the dark and the number of crossngs decreased. The effect ofshock among Trals 5-8 was analyzed by a two-way ANOVA wth repeated measures (treatment x trals). The changes were sgnfcant n all three parameters [latency-f(3,76) = 90.2, p <.001, F(3,228) = 65.8, P <.001, F(9,228) 18.8, P <.001; tme spent n the dark-f(3,76) = 97.6, p <.001, F(3,228) = 7.1, P <.01, F(9,228) = 1.86, n.s.; number ofcrossngs-f(3,76) = 32.96, p <.001, F(3,228) = 3.05, P <.05, F(9,228) = 0.41, n.s.; for latency, trals, and the nteracton n each case]. Group data obtaned n Trals 5-8 were compared across treatment effects usng the Duncan multple range test wth the between-groups error MS term of the overall ANOVA. Two sgnfcantly dfferent (p <.01), nonoverlappng ranges contanng the 100- and 75-rnA groups and the 50-rnA and control groups were found for latency and number of crossngs. In the case of tme spent n the dark, there were three sgnfcantly dfferent ranges: (1) the control group, (2) the 50-rnA group, and (3) the 75- and 100 rna groups. Analyss of Shock Trals 6-8 revealed consderable dfferences n the character of the three measured parameters. Only the effect of treatment was sgnfcant 900 '-' OJ OJ '" tl '-' " -'2 \ I /.j l/>r 100 ma_ 75mA -o- ""!, mA o_...:.::o_o!." 0 control trals Fgure 2. Increases n latency durng varous shock treatments. Group means ± SE are shown.

3 PARADISE FISH AVOIDANCE LEARNING 103 control 0 50mA ma <:> 100mA _ trals Fgure 3. Total tme spent n the dark durng varous treatments. Group means ± SE are shown ma... '" o 5 c:: con trol o ma _ 75 ma -ctrals Fgure 4. The number of gate crossngs durng varous treatments. Group means ± SE are shown. n both number of crossngs and tme spent n the dark [number of crossngs-f(3,76) = 30.65, P <.001, F(2,152) = 0.03, n.s., F(2,152) = 0.53, n.s.; tme spent n the dark-f(3,76) = 98.8, P <.001, F(2,152) = 2.6, n.s., F(6,152) = 1.2, n.s.; for treatment, trals, and the nteracton, respectvely, n each case]. Contrary to these fndngs, postshock changes n latency were sgnfcant not only for treatment shock ntensty but for trals and the nteracton as well [F(3,76) = 92.2, P <.001, F(2,152) = 11.63, P <.001, F(6,152) = 3.02, P <.00 I, for treatment, trals, and the nteracton, respectvely]. Dscusson Actve avodance condtonng s the most frequently used technque for studyng learnng n small rodents, such as mce and rats, and also n other speces, such as toads (Karplus, Algon, & Samuel, 1980) and goldfsh (Pnckney, 1967; Woodard & Btterman, 1971; Zerbolo & Wckstra, 1979). It has even been used on Macropodus operculars (Brookshre & Hognander, 1968). For our purpose, because ofproblems caused by the ntended use of the varous dummes, a passve avodance paradgm seemed better. In an actve avodance desgn, the dummy should also be shuttled between the compartments of the expermental chamber, but ths creates techncal problems. The am of Experment 1 was to nvestgate some parameters of the learnng process n paradse fsh n order to desgn the experments usng varous dummes. The parameters examned were latency, number ofcrossngs, and amount of tme spent n the dark. The three measures revealed dfferent aspects of the behavor of the paradse fsh n the present learnng stuaton. Latency showed a marked ncrease n groups treated

4 104 CSANYI wth 75- or loo-ma shock (Fgure 2). Ths was the only parameter that ncreased sgnfcantly day after day n the above groups, as revealed by the analyss ofthe postshock trals. Therefore, t can be assumed that an avodance learnng process was expressed most clearly n the latency parameter. Wth shock n the dark compartment, the fsh showed escape behavor, but the total tme spent n the dark changed only durng the frst shock tral (Fgure 3), correlatng roughly wth shock ntensty. Therefore, t s reasonable to suppose that ths parameter reflects the degree ofdscomfort n the shock compartment. It s also worth notng that the group shocked wth 50 rna had no sgnfcant ncrease n latency, but that the total tme spent n the dark fell to about 55% ofthat ofthe control group, and ths dfference was sgnfcant. The thrd parameter, the number ofcrossngs, also dd not show sgnfcant changes wth the second shock tral, and the mean values n the control and 50-rnA groups were very smlar, just as they were n the latency measure. Lester (1967,1968) observed that a mld ncrease n the fear level of rats ncreased ther exploratory tendency. Gate crossngs can certanly be vewed as a specal form of exploraton by the paradse fsh. Ths was also supported by other behavoral observatons. Before the gate crossngs were made, the fsh frequently orented toward the gate and lowered ther speed or stopped for a moment n front of the gate. Although mld shock of 50 rna sgnfcantly dmnshed the amount oftme spent n the dark compartment, thus showng the unpleasant nature of shock, t dd not change the number of crossngs sgnfcantly. Ths appears to be n agreement wth the results of Lester's (1968) experments wth rats. Our conclusons from Experment 1 are that a mld, 50 rna shock n ths passve avodance stuaton, whle beng clearly unpleasant, mantans exploraton and does not ntate observable learnng. Hgh-level shock promotes escape behavor, facltates learnng (expressed n ncreases n latency to enter the dark chamber), and nhbts exploraton, n agreement wth the fndngs of smlar studes usng other anmals. EXPERIMENT 2 In Experment 2, the effects of a mld shock (50 rna) and of the presence of varous dummes and of lve goldfsh from Tral 5 onward were examned. Method After the four habtuaton trals, 408 fsh were dvded nto 10 groups of varous szes, and from Tral 5 onward these groups were treated dfferently. In some treatments, varous dummes were placed n the back part of the dark compartment. The smplest of the dummes was a small red-lght lamp (LED), 4 mm n dameter, mounted on a pece of Plexglas connected to a small strp of lead so that t stood frmly on the bottom (dummy A; Fgure 5). Next n the seres were two smlar red lamps arranged ether vertcally (dummy B) or horzontally (dummy C). A more fsh-lke dummy was made from the head of a plastc toy fsh, wth two small red lamps substtuted for the eyes (dummy D). The last "dummy" was a lve adult goldfsh, 10 em long and large enough not to be able to leave the dark compartment through the gate. The dfferent dummes and 50-rnA shock were ntroduced n Tral 5 as follows: Groups 1-3 were not shocked. For Group 1 (n=20), no dummy was ntroduced. Group 2 (n= 18) had the goldfsh, and Group 3 (n=41) had dummy D. Groups 4-10 were shocked by 50 rna. For Group 4 (n=79), no dummy was used. Group 5 (n=20) had dummy D wthout ts lamps beng turned on-do. Group 6 (n=21) had dummy A; Group 7 (n=50), dummy B; Group 8 (n=52), dummy C; and Group 9 (n=71), dummy D. Group 10 (n=36) had the goldfsh. Results To compare the effects of the varous dummes, the group means of varous behavor parameters were calculated from the ndvdual averages of the last three trals, Trals 6-8, snce the last three postshock trals seemed to provde the most relable part of the ndvdual learnng curves. These averages are good ndcators of the anmal's avodance learnng (latency, Fgure 6), ts readness to escape (tme spent n the dark, Fgure 7), and ts tendency to explore (number of crossngs, Fgure 8). Avodance learnng, ndcated by hgh latency, showed a tendency to ncrease n groups shocked n the presence of dummes B, C, and D and the lve goldfsh. Statstcal analyss ofthe latences by one-way ANOYA for all 10 groups was hghly sgnfcant [F(9,398) = 27.7,! t O I ole ul 0 'r O.n(E I L tn*t -.lo mm mm I mm ' t- I 5E A B [ 0 I.nIE N,E - 4- Fgure 5. Varous dummes used n the passve avodance experments.

5 PARADISE FISH AVOIDANCE LEARNING 105 p <.001]. Post hoc comparsons of the means by Duncan range test (p <.05) revealed four dfferent, partally overlappng ranges, whch are shown n Fgure 6. Total tme spent n the dark also changed n the presence of some dummes. The one-way ANOVA for all 10 groups was sgnfcant [F(9,398) = 18.44, P <.001]. Four nonsgnfcant ranges (p <.05) were found by the Duncan multple range test. These are shown n Fgure 7. Exploraton reflected n the number of crossngs was also affected by the dummes. A one-way ANOVA for dummy: 0..c:: <5.!t.! c:: 0 g,... DO A B [ 0 Q <5.!t.! 5 g,... v + 50mA..c:: 900 <lj >-----; Duncan ranges 500 groups Fgure 6. Increase n latency n groups treated by varous dummes. Bars represent means ± SE; Duncan ranges are also shown. dummy: 0..c::: <5... '- c:: ll:; 0 <5... t:l1 900 s.s: <lj! loj 500 Do A B [ 0..c::: <5 c:: :l;l 0... rr g, Q v +50mA t---l Duncan ranges groups Fgure 7. Tme spent n the dark by groups exposed to varous dummes. Bars represent means ± SE; Duncan ranges are also shown.

6 106 CSANYI all groups was hghly sgnfcant [F(9,398) = 10.28, p <.001]. A Duncan range test (p <.05) revealed the three nonsgnfcant ranges shown n Fgure 8. Observaton of the fshes revealed characterstc dfferences n overt behavor among the groups. Subjects n the groups treated wth both shock and wth dummy C, dummy D, or the goldfsh (Groups 8, 9, and 10) swam out very quckly from the dark compartment after beng shocked and then usually turned back mmedately, swam to the gate, and spent consderable tme lookng nto the dark compartment. The fsh n the other groups just came out normally and went nto the dark agan wthout any hestaton. In the groups treated wth both goldfsh and' shock, the goldfsh tself also receved the shock and reacted wth frequent jumps and rushes. Ths behavor certanly rased the dscomfortng features of the dark compartment for the paradse fsh. Dscusson These results ndcate that the presence of fsh-lke dummes enhances the effect of a mld shock on all three parameters. On latences, lve fsh exert the greatest effect (Group 10; Fgure 6). Next n effect, after the goldfsh, s the most fsh-lke dummy, D (Group 9), although dummy C has almost the same effect (Group 8), demonstratng that the most mportant propertes of these dummes are the two lateral eye-lke spots provded by the lamps. The effects of dummy Do, wthout lamps (Group 5), and dummy A, whch had only one lamp (Group 6), were not sgnfcantly dfferent from that of the control. Thus, two lateral eyespots certanly have a key-stmulus character. Even the confguraton ofthe two spots seems to be mportant, snce the horzontal arrangement (Group 8) s sgnfcantly better at rasng latency than s the vertcal one (Group 7). Ths fndng s certanly not unque: It s well known that eyespots nduce avodance behavor n certan small mammals (Coss, 1978b), brds (Blest, 1957; Jones, 1980), and fsh (Coss, 1979). As Experment 1 showed, total tme n the dark reflected readness to escape as a result of the dscomfort of the treatments. Experment 2 seemed to show that dummy D wthout shock (Group 3) exerted no unpleasant effect and that a lve companon goldfsh wthout shock (Group 2) was almost as uncomfortable as mld shock alone (Group 4). In general these no-shock groups tend not to dffer from the no-shock no-dummy control (Group 1). If both shock and dummy D or the goldfsh are present (Groups 9 and 10), the dscomfort ofthe treatments s greatly enhanced, as shown by the sgnfcant decrease of total tme n the dark. The components of the "dscomfort' exerted by the dummes and mld shock are at least of two knds. The frst s clearly the pan caused by the shock, whch s ndependent of the presence or absence of the dummes (Groups 1 and 4), and the other s most probably fear. The nfluence ofthe fear component s not observed when the dummes have been presented wthout shock because the total tmes n the dark are almost the same for the control and the dummy groups (Groups 1 and 3) n ths condton. The most plausble explanaton s that the dummes do have fear-elctng propertes, but only n the presence of a mld pan. The same can be sad for lve goldfsh (Csany, 1985). The effect of the dummes on the number ofcrossngs dffers from ther effect on the tme spent n the dark. The dummy: V). V) V) c c, 10 -<::: c;.\!!.t: : c "'" 5 '-' D Do A B [ D -<::: c;.t: :l::! 5 c '-' v + 50 ma "'" Duncan ranges '-' ClJ... t:l "'" groups Fgure 8. The number of gate crossngs n groups exposed to varous dummes. Bars represent means ± SE; Duncan ranges are also shown.

7 PARADISE FISH AVOIDANCE LEARNING 107 number of crossngs does not dffer among the frst four groups, two of whch (Groups 2 and 4) showed a consderable decrease n total tme n the dark, evdencng the dscomfort of the treatment. Ths result supports the assumpton that mldly unpleasant treatments mantan exploratory behavor. EXPERIMENT 3 The am of Experment 3 was to examne the reversblty of the effect of fsh-lke dummes on the enhancement of latency, the parameterby whch learnng s seemngly best reflected n ths passve avodance learnng stuaton. Shock of 100 rna was used, because t was, by tself, effectve enough to elct consderable avodance behavor n Experment 1. Method Forty fsh were dvded nto four groups after the habtuaton trals. Group I (n= 10) served as control, wth nether shock nor dummes appled. Group 2 (n= 10) was shocked wth 100 rna but had no dummy present. Group 3 (n=10) had dummy Dand was shocked wth 100 rna from Tral 5 through Tral 11; on Trals 12, 13, and 14, the dummy was removed and the shock was omtted. Group 4 (n= 10) was treated lke Group 3, but the dummy was replaced on Tral 14. Results and Dscusson The results are shown n Fgure 9. Treatment wth 100 rna shock alone and loo-ma shock wth dummy D quckly enhanced the latency, and there was no sgnfcant dfference between the two treatments. Latency decreased consderably when both the dummy was removed and the shock was omtted (Groups 3 and 4 on Trals and 12-13, respectvely). Latency ncreased agan when the dummy was placed back but shock contnued to be omtted (Group 4, Tral 14). The effect of the dummy removal was sgnfcant, as revealed by an ANOVA. Trals were compared by two-way ANOVA wth repeated measures (treatment x trals) for all groups and separately for the shocked groups (Groups 2, 3, and 4). The dfferences were hghly sgnfcant [treatments, F(3,36) = 67.5, P <.001, and F(2,27) = 35.9, P <.001; trals, F(2,72) = 6.68, P <.01, and F(2,54) = 6.67, P <.01; nteractons, F(6,72) = 13.23, P <.001, and F(4,54) = 14.15, P <.001]. Some parwse comparsons were also made. Dfferences were sgnfcant for treatment between Groups 2 and 3 [F(1,18) = 72.6, P <.001, F(2,36) = 2.68, n.s., and F(2,36) = 2.68, n.s., for treatment, trals, and nteracton, respectvely]. In a comparson of Group 3 and Group 4, dfferences n all three parameters were sgnfcant [F(1,18) = 5.83, P <.05, F(2,36) = 6.65, P <.01, F(2,36) = 16.6, P <.001, for treatment, trals; and nteracton, respectvely]. For Tral 14, Groups 3 and 4 were compared by one-way ANOVA. The dfference was sgnfcant [F(1,18) = 115.4, P <.001]. Ths experment supports the assumpton that, wth a fsh-lke dummy present, the panful experence of the shock was assocated by the subjects wth the dummy. Wthout the dummy, t was the physcal cues of the dark compartment that exerted a long-lastng effect on behavor. Fsh belongng to the latter group completely avoded the dark compartment on the last fve trals. The effect of the dummy n ths experment can also be explaned by the noton of an overshadowng of contextual stmul by a more salent, bologcally relevant stmulus (Rescorla, 1968; Wagner, 1969)..-. control.--. empty dummy I no shock 100 ma shock 900 ClJ trals Fgure 9. Latency tme durng manpulaton wth dummes. Arrows pont to the tralsthatwere followed by removal and replacementof the dummy n the respectve groups. Means ± SE are shown.

8 108 CSANYI GENERAL DISCUSSION Varous psychologcal schools have nvested enormous effort n the search for a general theory of learnng. Although ths lne of nvestgaton has revealed a great many facets of the anmal learnng process and has led to the dscovery of very effectve tranng methods, the theores and belefs underlyng the generalzed psychologcal approach has been serously questoned durng the last 20 years by researchers who started to emphasze the varous constrants of nstrumental and classcal condtonng (Garca & Koellng, 1966; Rozn & Kalat, 1972; Selgman, 1970; Selgman & Hager, 1972). The bulk of the evdence n favor of the bologcal boundares approach has been provded by taste-averson learnng, but studes of other forms of learnng, such as nstrumental avodance n rats (Bolles, 1970) and complementary data usng food renforcement n an operant condtonng paradgm wth hamsters (Shettleworth, 1972) also showed speces-specfc "bologcal constrants" on the anmal's learnng ablty. The dscovery of the constrants-onlearnng phenomena successfully undermned the prncple of equpotentalty, whch, although t had never been explctly beleved, greatly nfluenced the thnkng of students n ths feld. The other pnnacle of the psychologcal theory, namely the vew that all nstances of assocatve learnng nvolve the same basc underlyng process, was very lttle challenged by the constrants-on-learnng phenomena (Roper, 1983). A few researchers, rather than abandonng the search for general laws of learnng, responded by attemptng to formulate somewhat restrcted new "laws" to accommodate the phenomena oflearnng constrants (Revusky, 1977), or tred to ntegrate the speces-specfc nstances of learnng nto the tradtonal framework of the psychologcal theory on the bass of a general process approach (Domjan & Galef, 1983). In my opnon, the crucal problem s not whether the nstances of assocatve learnng nvolve the same underlyng process, or even the valdty of the prncple of equpotentalty, but the specfc relatonshps of the assocatve process(es) to the gven speces-specfc behavoral system, the mportance of whch unfortunately has not been recognzed by the general process approach. Learnng may be vewed as a specal means of adaptaton, an ablty evolved by anmals n the course of evoluton, whch can be properly studed only by consderng the close and dynamc relatonshp between the behavor repertore of a gven speces and ts envronment (Johnston, 1981, 1982). The varous forms of learnng may be consdered as parts ofthe ethogram n the same way as the genetcally better defned, less flexble behavor patterns. The most ethologcally orented theory of aversve condtonng was constructed by Bolles (Bolles, 1970; Bolles & Fanselow, 1980). The prncpal clams of ths theory are the followng: Any stmulus that causes fear elcts speces-specfc defense reactons (SSDR) uncondtonally. If the uncondtoned stmulus s accompaned by a contguous, neutral stmulus, then, after some repetton, the condtoned stmulus alone s capable of elctng the SSDR. And avodance learnng could occur rapdly only f the requred response was one of the anmal's SSDRs. If we apply ths smple model to the case of passve avodance condtonng n the paradse fsh, t fts the observatons only very roughly. Hgh-ntensty shock elcts specfc escape reactons n the paradse fsh, and, f the experence s repeated, the features of the place where the shock occurred are enough to actvate the passve avodance response. The desgn of the apparatus used n ths experment was approprate for the study of the avodance reacton, measured as the ncrease n latency, that s, the escape reactons reflected n tme spent n the dark. Besdes some agreement wth Bolles's model, there are two mportant features ofthe behavor of paradse fsh whch suggest the need for consderable modfcaton of the model. If the anmal s shocked by a relatvely mld, but clearly unpleasant, shock, t mantans exploraton, and ths s generally not ncluded among SSDRs. Such exploratory behavor n these experments was ndcated by the large number of gate crossngs. Our prevous observatons of the nteractons of paradse fsh and a lve predator (Csany, 1985) also showed that a nave paradse fsh or one rased n solaton reacts to the sght of a predator by actve exploraton. A shock of hgh ntensty or an attack by the predator lowers ths tendency to explore. The second mportant feature of these experments was that the presence ofeyespot-lke stmul greatly nfluenced the exploratory behavor of paradse fsh treated by mld electrc shocks. Although a mld shock was neffectve f appled alone, mld shock and an eyespot model together led to avodance condtonng. Any smple explanaton by senstzaton was ruled out because the stmul were hghly specfc. Besdes lve fsh, only two laterally arranged spots were sutable for avodance condtonng (Experment 2), and avodance was mantaned by the presence of the approprate stmul even f shock level was hgh enough to elct avodance alone (Experment 3). These results are very smlar to prevous ones (Csany, 1985) that showed that a harmless goldfsh can be turned nto an object that s actvely avoded by the paradse fsh when a mld shock s appled to the paradse fsh n the goldfsh's presence. To account for the man features of the paradse fsh's learnng, Bolles's model must be suppled wth a new feature. Ths new feature s the speces-specfc key-stmulus (SSKS). Upon the appearance of such stmul n the envronment of the paradse fsh, an dentfcaton process starts and results n mmedate orentaton and thorough exploraton. Ifthe carrer of the key stmul s passve, then the exploratory behavor slowly dmnshes by way of habtuaton. If the carrer of the SSKS nteracts wth the paradse fsh and causes fear or pan, then the SSDR becomes actvated and the exact features of the carrer become fxed n memory by S-S-type assocatons. If the same stmul recur, then the SSDR becomes elcted by ts representaton n memory wthout the need for exploraton.

9 PARADISE FISH AVOIDANCE LEARNING 109 Bolles and Fanselow (1980), n ther descrpton of avodance condtonng, placed emphass on the role of fear as the man organzer of behavor n the learnng stuaton. Our experments supplement ths concepton by suggestng an mportant organzatonal role for SSKSs. SSKSs drect the assocaton process: they sgnal whch objects n the envronment are worth thorough exploraton and whch features must be assocated wth the concurrently occurrng pan or fear. In a new envronment, the anmal s contnuously searchng for the approprate SSKSs that are the organzatonal focal pont of ts defensve behavor. An mportant functon of the anmal's bran s the dynamc representaton of ts envronment wth whch t can predct events relevant to ts survval. It can be safely assumed that the bran of the paradse fsh has a genetcally determned predsposton n the form of a crude "mental template," whch drects exploraton of the envronment and, upon encounters wth SSKS carrers, renders dentfcaton possble. In the natural envronment, where both harmless and predatory carrers of SSKS can be found, encounters wth predators may result n chase or panful njury, whch ntates a learnng process that results n a representaton, n the paradse fsh's bran, of the actual features of a gven predator. Ths representaton acts as an organzer of behavor n subsequent encounters. The paradse fsh lves n small ponds and streams, where the numbers of the possble predator speces are certanly under some lmts. Occasonal meetng wth one of them results n an SSKS-drected learnng process whch, throughout the entre lfe of the anmal, creates a network of the representaton of the approprate predator. Ths very network can be regarded as a dynamc model of the gven envronment. The dynamcs of ths model results n avodance behavor by the paradse fsh f, and only f, t s necessary-that s, only n the case of the appearance of the predator. The ablty to rely on ths model certanly fulflls the crtera of the ablty to predct. 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