Functional class formation in the context of a foraging task in capuchin monkeys

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FUNCTIONAL CLASS FORMATION IN THE CONTEXT OF A FORAGING TASK IN CAPUCHIN MONKEYS ROMARIZ DA SILVA BARROS 1 ,CARLOS BARBOSA ALVES DE SOUZA 1 , AND THIAGO DIAS COSTA 2 1 UNIVERSIDADE FEDERAL DO PARÁ, PROGRAMA DE PÓS-GRADUAÇÃO EM TEORIA E PESQUISA DO COMPORTAMENTO 2 UNIVERSIDADE FEDERAL DO PARÁ, FACULDADE DE PSICOLOGIA Functional class formation via repeated reversals of simple discriminations was investigated in a foraging task in captive capuchin monkeys (Cebus cf. apella). Two capuchin monkeys were given simultaneous simple discrimination training and reversals with two (Phase 1), four (Phase 2), and six (Phase 3) visual stimuli (wooden boxes) in the context of searching for food in an apparatus. One different kind of food for each potential stimulus class was used as a reinforcer. After repeated functional reversals of two stimulus sets, multiple tests for functional class formation were performed (Phase 4). Evidence of class formation was found in all of the tests. Next, the same monkeys were given simultaneous simple discrimination training with variations of the stimulus locations between sessions (Phase 5). The class-specific reinforcement procedure was suspended. Tests for functional class formation were again performed. Evidence of class formation was found in all tests. The data suggest that some of the procedural difficulties in documenting class formation in nonhumans can be overcome with procedures that take advantage of the natural skills of the subjects. Key words: simple discriminations, reversals, functional classes, Cebus cf. apella According to Vaughan (1988), equivalence relations between elements of a stimulus set can be viewed as a behavioral analogue of the mathematical concept of partition. Given, for example, a certain stimulus set, a partition is a set of disjoint subsets of the set, with the union of those sets equating the original set(p. 36). Vaughan (1988) published the first report of functional class formation with six experimen- tally naïve pigeons as subjects. In that study, simple discriminations were trained with two stimulus subsets. That is, 40 pictures of trees were each randomly assigned to one of two subsets of 20 pictures each. Within a session, all of the stimuli in a subset had the same stimulus function. Stimuli in one subset served as an S þ for pecking and stimuli in the other subset served as S - . Following the acquisition of discriminated responding, 160 discrimination reversals were conducted in which the function assigned to the subsets (S þ or S - ) were reversed. By the end of the experiment, when the pigeons experienced a functional reversal with some of the stimuli in a subset, their responding to the remaining stimuli in the subset changed. That is, other stimuli in the subset, when encountered for the first time in the session, functioned as S þ or S - depending on the within-session function of other stimuli in this subset. Vaughan did not conduct probe trials to test for functional class formation. Instead, he inferred this result based on how early, following a reversal, that the pigeons showed discrimination reversal. Thus, Vaughan (1988) documented, in the pigeon, the capability of dividing a large stimulus set into two disjoint subsets of function- ally equivalent stimuli. This was termed function- al class formation because the elements of a subset shared a (discriminative) function. Based on these data, Vaughan proposed the existence of equivalence relations between elements of a stimulus subset as a behavioral analogue of the mathematical concept of partition. Functional class formation via a simple discrimination reversal procedure is difficult to document in nonhuman subjects (e.g., Dahás, Brasiliense, Barros, Costa, & Souza, 2010; Dube, Callahan, & McIlvane, 1993; This research is part of the National Institute of Science and Technology on Behavior, Cognition, and Teaching (CNPq grant 573972/2008-7 and FAPESP grant 2008/57705- 8). It was also supported by CAPES (Coordination for the Development of Graduated Personnel - Brasília, Brazil - PhD scholarship for the last author), CNPq (National Council for Scientific and Technological Development - Brasília, Brazil - grants 406307/2006-7, 473479/2006-0, and 314425/2009-8), National Institute of Health. Data reported here come in part from Costas PhD dissertation supervised by Dr. Barros in the Graduate Program on Theory and Research on Behavior at Federal University of Pará. We thank William Dube, William McIlvane, and Olavo Galvão for discussing previous versions of the present work. Address correspondence to Romariz Barros, Federal University of Pará, R. Augusto Correia, 01, Belém, PA, Brazil, 66.075-110 (e-mail: [email protected]). doi: 10.1002/jeab.27 JOURNAL OF THE EXPERIMENTAL ANALYSIS OF BEHAVIOR 2013, 100, 7987 NUMBER 1 (JULY) 79

Transcript of Functional class formation in the context of a foraging task in capuchin monkeys

FUNCTIONAL CLASS FORMATION IN THE CONTEXT OF A FORAGING TASK INCAPUCHIN MONKEYS

ROMARIZ DA SILVA BARROS1, CARLOS BARBOSA ALVES DE SOUZA

1, AND THIAGO DIAS COSTA2

1UNIVERSIDADE FEDERAL DO PARÁ, PROGRAMA DE PÓS-GRADUAÇÃO EM TEORIA E PESQUISA DO COMPORTAMENTO2UNIVERSIDADE FEDERAL DO PARÁ, FACULDADE DE PSICOLOGIA

Functional class formation via repeated reversals of simple discriminations was investigated in a foragingtask in captive capuchinmonkeys (Cebus cf. apella). Two capuchinmonkeys were given simultaneous simplediscrimination training and reversals with two (Phase 1), four (Phase 2), and six (Phase 3) visual stimuli(wooden boxes) in the context of searching for food in an apparatus. One different kind of food for eachpotential stimulus class was used as a reinforcer. After repeated functional reversals of two stimulus sets,multiple tests for functional class formation were performed (Phase 4). Evidence of class formation wasfound in all of the tests. Next, the same monkeys were given simultaneous simple discrimination trainingwith variations of the stimulus locations between sessions (Phase 5). The class-specific reinforcementprocedure was suspended. Tests for functional class formation were again performed. Evidence of classformation was found in all tests. The data suggest that some of the procedural difficulties in documentingclass formation in nonhumans can be overcome with procedures that take advantage of the natural skills ofthe subjects.Key words: simple discriminations, reversals, functional classes, Cebus cf. apella

According to Vaughan (1988), equivalencerelations between elements of a stimulus set canbe viewed as a behavioral analogue of themathematical concept of partition. Given, forexample, a certain stimulus set, a partition is “aset of disjoint subsets of the set, with the union ofthose sets equating the original set” (p. 36).Vaughan (1988) published the first report of

functional class formation with six experimen-tally naïve pigeons as subjects. In that study,simple discriminations were trained with twostimulus subsets. That is, 40 pictures of treeswere each randomly assigned to one of twosubsets of 20 pictures each. Within a session, allof the stimuli in a subset had the same stimulusfunction. Stimuli in one subset served as an Sþ

for pecking and stimuli in the other subsetserved as S−. Following the acquisition ofdiscriminated responding, 160 discriminationreversals were conducted in which the functionassigned to the subsets (Sþ or S−) were reversed.By the end of the experiment, when the pigeonsexperienced a functional reversal with some ofthe stimuli in a subset, their responding to theremaining stimuli in the subset changed. That is,other stimuli in the subset, when encounteredfor the first time in the session, functioned as Sþ

or S− depending on the within-session functionof other stimuli in this subset. Vaughan did notconduct probe trials to test for functional classformation. Instead, he inferred this result basedon how early, following a reversal, that thepigeons showed discrimination reversal.Thus, Vaughan (1988) documented, in the

pigeon, the capability of dividing a largestimulus set into two disjoint subsets of function-ally equivalent stimuli. This was termed function-al class formation because the elements of a subsetshared a (discriminative) function. Based onthese data, Vaughan proposed the existence ofequivalence relations between elements of astimulus subset as a behavioral analogue of themathematical concept of partition.Functional class formation via a simple

discrimination reversal procedure is difficultto document in nonhuman subjects (e.g.,Dahás, Brasiliense, Barros, Costa, & Souza,2010; Dube, Callahan, & McIlvane, 1993;

This research is part of the National Institute of Scienceand Technology on Behavior, Cognition, and Teaching(CNPq grant 573972/2008-7 and FAPESP grant 2008/57705-8). It was also supported by CAPES (Coordination for theDevelopment of Graduated Personnel - Brasília, Brazil - PhDscholarship for the last author), CNPq (National Council forScientific and Technological Development - Brasília, Brazil -grants 406307/2006-7, 473479/2006-0, and 314425/2009-8),National Institute of Health. Data reported here come inpart from Costa’s PhD dissertation supervised by Dr. Barrosin the Graduate Program on Theory and Research onBehavior at Federal University of Pará. We thank WilliamDube, William McIlvane, and Olavo Galvão for discussingprevious versions of the present work.Address correspondence to Romariz Barros, Federal

University of Pará, R. Augusto Correia, 01, Belém, PA,Brazil, 66.075-110 (e-mail: [email protected]).doi: 10.1002/jeab.27

JOURNAL OF THE EXPERIMENTAL ANALYSIS OF BEHAVIOR 2013, 100, 79–87 NUMBER 1 (JULY)

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Goulart, Galvão, & Barros, 2003; see also Barros,Picanço, Costa, & Souza, in press), with a studyof sea lions (Kastak, Schusterman, & Kastak,2001) serving as the only convincing demon-stration of functional class formation afterVaughan (1988). Functional class formationhas also been difficult to document in humanswith severe developmental disabilities (Lionello-DeNolf, McIlvane, Canovas, Souza, & Barros,2008, Experiment 2; Sidman, Wynne, Maguire,& Barnes, 1989; see also Canovas, Souza, &Barros, in press) and in typically developingyoung children (Lionello-DeNolf et al., 2008,Experiment 1; see also Canovas, 2010).

The present research was concerned withprocedural variables that may facilitate func-tional class formation. We hypothesized that thesuccess of training functional class formationcould be improved by using a task that iscompatible with the phylogenetic skills of thespecies. Because we used capuchin monkeys(Cebus cf. apella), a species well known for theirefficiency in searching for food (Sampaio, 2004)and for their ability to discriminate locationswhere food has and has not been previouslyfound (De Lillo, Aversano, Tuci, & Visalberghi,1998; Garber & Paciulli, 1997; Janson, 1998;Pot, 2000), we arranged a foraging task to studyfunctional class formation. In addition, in thenatural environment capuchins adjust theirforaging behavior to seasonal variations thatimply changes in the availability of food (Brown& Zunino, 1990; Phillips, 1995; Siemers, 2000).Specifically, they increase the time that theysearch for tubers and insects during dry seasonsand increase the time that they search for fruitsduring rainy seasons (Rímoli, 2001; Siemers,2000; Terborgh, 1983). To capitalize on thisspecies’ sensitivity to the availability of differentfoods, we arranged class-specific food rein-forcers; a procedure that Kastak et al. (2001)employed with sea lions and which theyhypothesized may facilitate functional classformation (see also Sidman, 2000). Additionally,several studies have reported that discrimina-tion training with primate subjects is facilitatedwhen three-dimensional stimuli are used (Limaet al., 2007; Oden, Thompson, & Premack, 1988;Souza, Borges, Goulart, Barros, &Galvão, 2009).Therefore, the stimuli in our subsets were three-dimensional wooden boxes.

Finally, we employed a probe procedure thatwas developed by Dube et al. (1993). Specifical-ly, to test for functional class formation following

a reversal of the Sþ/S− functions of the stimuliwithin a set, Dube et al. allowed subjects toacquire the new functions with two of the threestimuli in each set. When the discriminationreversal was learned with these two stimuli, thewithheld stimulus from each set was reintro-duced in unreinforced probe trails.

In our procedure, repeated reversals ofsimple discriminations were trained with sixwooden boxes as stimuli. Three boxes containedfood (Sþ) and three were empty (S−). Trainingstarted with two boxes, one baited with food andthe other empty (Phase 1). When the monkeysmastered this discrimination and subsequentreversals, new pairs of boxes were added, onepair at a time (Phases 2 and 3). Tests forfunctional class formation were carried outin Phase 4 using the probe procedure ofDube et al. (1993). Phases 3 and 4 weresystematically replicated (in Phase 5) using amodified procedure that prevented control bylocation or conditional control by class-specificconsequences.

Methods

SubjectsTwo capuchin monkeys (Cebus cf. apella) were

used in the study. Adam (M18) was an adultmale (5 years and 7months old at the beginningof the experiment) with experience withrepeated reversals of simple discriminationsand identity-matching-to-sample with shapespresented on a computer screen, and with smallobjects (Souza et al., 2009). Tico (M23; 3 yearsand 6 months old at the beginning of theexperiment) had prior experience with acomputer-based identity-matching-to-sampleprocedure (Man, 2007). None of the monkeyshad any experience with the apparatus used inthe present study.

Experimental Environment and StimuliThe subjects were housed with other monkeys

4 or 5 to a cage that measured 2.50 � 2.50� 2.50 m. The cages were made of a galvanizedsteel screen welded on a galvanized steel cubiclestructure assembled on a concrete floor. Half ofthe ceiling was covered with tiles made of clay.Five separation cages (0.60 � 0.50 � 0.50 m)were attached to one of the walls of thehomecage. The separation cages were used (i)when the monkeys were individually fed, (ii)

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when the homecage was being cleaned, and (iii)during the experimental sessions to separate theexperimental subject from the other animals.Monkeys M18 and M23 lived in separate homecages with other conspecifics.The monkeys were fed twice per day with

fruits, vegetables, tubers, eggs, vitamins, andmilk. They had free access to water. A veterinar-ian provided health and nutritional assistance.The housing facilities, handling, and experi-mental procedures used were in accordancewith local and international regulations andapproved by the National Institute for Environ-mental Issues (IBAMA) and Animal ResearchEthical Committee of the Federal University ofPará, Brazil.The apparatus consisted of six different

colored wooden boxes (0.32 � 0.17 � 0.14 m)attached to a vertical wooden structure(1.75 � 1.27 m) assembled on a platform withfour small wheels so that the entire apparatuscould be easily placed close to the home cage.Each box had an opening on the front wall thatprovided access to its contents. A small plasticcurtain prevented the monkeys from seeing thecontents of the box. Another opening on theback wall of the box allowed the experimenter toplace food in a small bowl inside the box.The six boxes were arbitrarily divided into two

sets. Six fruit replicas (papaya, coconut, pinecone, apple, watermelon, and star fruit) made ofwax were attached, one on top of each box, toenhance discriminability. Set 1 consisted of A1(blue box, with a replica of papaya), B1 (yellow,coconut), and C1 (black, apple). Set 2 consistedof A2 (red, pine cone), B2 (green, watermelon),andC2 (purple, star fruit). The boxes were hungon the wooden structure in six differentpositions (displayed as a matrix of two columnsand three rows), 0.77 m from each otherhorizontally and 0.48 m from each othervertically. The position of each box was alwaysthe same throughout Phases 1 to 4 (from the topto the bottom, and from the left to the right,position 1 ¼ A1; position 2 ¼ C2; position3 ¼ A2; position 4 ¼ B1; position 5 ¼ C1;position 6 ¼ B2) and varied from session tosession in Phase 5. We acknowledge thatpresenting the stimuli always in the samelocation may allow the development of adventi-tious control by stimulus location; nevertheless,the procedure was inspired by the idea thatsources of food in the natural environment,such as trees, are always in the same location

(see for example, Garber & Paciulli, 1977). Thepotential influence of stimulus location wasevaluated in Phase 5.A food preference test (Fisher et al., 1992)

among dry food items was performed with eachmonkey to determine the items to be used asconsequences for correct responses. The toptwo preferred food items (crackers and choco-late cereal) were used.

ProcedureExperimental sessions were performed once

per day, Monday to Friday, approximately 1 hrbefore the main meal. This schedule did notrequire any deprivation procedure that mightresult in weight loss. Before each session, all ofthe monkeys in the home cage, with theexception of the experimental subject, weremoved to the separation cages. The experimen-tal sessions consisted of 20 discrete trials ofsimple discrimination training. Each trial beganwhen the apparatus was placed near the homecage, allowing the monkey to choose among theavailable boxes. After the choice responses, theapparatus was moved away from the home cage,and the trial ended. The intertrial interval (ITI)was approximately 15 s, varying according to thetime necessary for the experimenter to placefood in the wooden boxes. The experimenterwas always positioned behind the apparatus andplaced the food into the boxes through theopening on the back of each box. Additionally,while placing the food in the wooden boxes, theexperimenter always put his hand with food intoall of the boxes, but he placed food only in theboxes assigned as Sþ such that (i) there was foodsmell in all boxes; (ii) no visual cue of the food’slocation was provided (i.e., the manipulation ofa box by the experimenter was never correlatedwith food availability in that box) and (iii) theITI did not vary greatly between experimentalphases as a function of the number of boxes withfood.A choice response consisted of hand insertion

into the box. Looking at the box or touching iton the outside was not considered a choiceresponse. On trials in which the monkeyselected the Sþ without error, an additionalpiece of food (i.e., bonus) was given by anotherexperimenter close to the opposite wall of thehomecage. The bonus was a piece of the samefood available in the Sþ boxes. Reaching intoany of the S− boxes, even after obtaining foodfrom the Sþ boxes, produced an immediate end

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of the trial (initiating the ITI) with no bonus.The function of the bonus was, then, todiscourage subjects frommaking an S− responseafter having chosen all available Sþ.

The responses were manually recorded dur-ing the sessions by the experimenter whodelivered bonus pellets. All the experimentalsessions were videotaped. The manual recordswere always carefully checked by the otherexperimenter (using the videotape) and, ifnecessary, corrected after each session. Theaccuracy of the manual record was over 95%.Data were analyzed only after being corrected.

The acquisition criterion was six consecutivetrials in which the monkey selected all availableSþ boxes and then moved away from theapparatus without reaching into any of the S−

boxes. Sessions ended after 20 trials or when theacquisition criterion was reached, whicheveroccurred first.

Throughout Phases 1 to 4, when any of thestimuli from Set 1 (A1, B1, or C1) functioned asthe Sþ, correct responses produced access tochocolate cereal. When any of the stimuli fromSet 2 (A2, B2, or C2) functioned as the Sþ,correct responses produced access to crackers.

Phase 1. Two-choice simple discrimination train-ing. Phase 1 consisted of training four differentsimple discriminations: A1þ/B2−, B2þ/B1−,B1þ/A2−, and A2þ/A1− with just two boxespresented on each trial. Training began with theA1 þ /B2- box arrangement, and training withthis arrangement continued across sessions untilthe acquisition criterion was met. Choosing theSþ was reinforced with presentation of thecorresponding food item and an auditoryprompt (i.e., whistle) that indicated the avail-ability of the bonus. If, after the response to theSþ and prompt presentation, the monkeymoved away from the apparatus, then the bonuswas presented. Reaching into the S− box endedthe trial with no access to food. The promptpresentation was faded over the course ofPhase 1.

When the acquisition criterion was reachedwith a single box-arrangement (e.g., A1þ/B2−),the session was ended and the Sþwas not used inthe next session; instead, the prior S− becamethe Sþ, and a new stimulus was presented as theS− (e.g., B2þ/B1−). This phase ended when themonkeys met the acquisition criterion with allfour single box-arrangements.

Phase 2. Four-choice simple discrimination train-ing. In Phase 2, all four stimuli presented over

the course of Phase 1 were presented simulta-neously in each trial. When A1 and B1functioned as the Sþ (boxes baited with choco-late cereal), A2 and B2 functioned as the S− andvice-versa. When A2 and B2 functioned as theSþ, correct choices were followed by access tocrackers. Responding was scored as correct on atrial when the monkey reached into only the Sþ

boxes and thenmoved away from the apparatus;the bonus reward was provided on correct trials.After the acquisition criterion was met with oneSþ/S− arrangement, these contingencies werereversed. Phase 2 ended after the acquisitioncriterion was met on the eighth discriminationreversal. Due to experimenter error, monkeyM18 was given an extra reversal.

Phase 3. Six-choice simple discrimination train-ing. In Phase 3, all six stimuli were presentedsimultaneously. Boxes A1-C1 were baited withchocolate cereal when these functioned as Sþ

stimuli, and boxes A2-C2 were baited withcrackers when they functioned as Sþ stimuli.Responding was considered correct within atrial if the monkey selected the three Sþ boxesand then moved away from the apparatuswithout reaching into an S− box. If thatoccurred, then the monkey received a bonusas described above. As before, choice metthe acquisition criterion (i.e., six consecutivecorrect trials, each composed of three selectionsof Sþ) before reversals were implemented. Ifthis criterion was not reached in a 20-trialsession, then the same training contingencieswere presented in the next session, thenext day. When the criterion was reached, thesession was interrupted, and reversed contin-gencies were presented in the next session(next day).

Phase 3 ended when fast acquisition of thereversed discrimination was observed at leasttwice. Fast acquisition was operationalized asfollows: After the Sþ/S− functions were reversed,the first response in the first trial was nearlyalways incorrect and this response ended thetrial (apparatus was pulled away from the cageand the ITI sequence was initiated as describedabove). On a subsequent trial (not necessarilythe next trial) the monkey would choose an Sþ

box (first choice response in the trial) andobtain a food reward. If the second choice in thetrial was another Sþ box, then fast acquisitionwas demonstrated.

This can be illustrated by the followingsituation: consider A2, B2, and C2 functioning

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as Sþ, and A1, B1, and C1 as S−, following acontingency reversal. A monkey may respondinitially to A1−, B1−, or C1− (the usualpostreversal error) but eventually the monkeyresponds to, for example, B2þ (i.e., the firstcorrect response in a trial). If the next choiceresponse was to A2þ or C2þ, then this wasconsidered evidence of fast reversal acquisition.Additionally, the maintenance of responding tothe new Sþwas evaluated throughout the sessionso that the acquisition criterion of six consecu-tive correct trials could be reached in as little asseven total trials.Phase 4. Tests for functional class formation.

During this phase, a new discrimination reversalwas initiated with only four stimuli presented(e.g., A1þ and B1þ; A2− and B2−). When theacquisition criterion was reached with the fourstimuli, on the next trial, in the same session, thetwo previously withheld stimuli (e.g., C1 andC2)were reintroduced along with the other four.Selecting the Sþ box was reinforced on these testtrials. Test sessions continued for 20 trials oruntil six consecutive correct trials were re-corded. Across sessions, six different tests forfunctional class formation were performed.Each test was conducted after the acquisitioncriterion had been satisfied with four stimuliafter the reversal of Sþ/S− assignments. The testsfor functional class formation are here identi-fied by the withheld stimulus pair: A1þ/A2−,B2þ/B1−, C1þ/C2−, A2þ/A1−, B1þ/B2−, andC2þ/C1−.The first choice of one of the two withheld

stimuli was critical for the analysis of functionalclass formation. If the response was consistentwith the reversed contingencies (e.g., after thefunction of A1 and B1 had been reversed to Sþ,the monkey selected the newly presentedC1 instead of C2) then that was consideredpositive evidence of functional class formation.Performance indicative of functional classformation had to be obtained in the first testtrial of at least five of the six test sessions.Phase 5. Tests for functional class formation with

variations of stimulus locations. The same generalprocedure described in Phases 3 and 4 was usedin Phase 5 with two exceptions: (i) there was noclass-specific reinforcement: we replaced crack-ers and cereal with sweet popcorn; (ii) allstimulus locations changed between sessions.The purpose of Phase 5 was to determine if theunchanged stimulus location was a criticalvariable for the results found in Phase 4. We

also checked if responding in a given trial wasin some measure based on conditionalcontrol by the reinforcer presented in a previoustrial.Phase 5 began with simple discrimination

reversal training with all six stimuli. When theacquisition criterion was reached, the experi-mental session was terminated. In the nextsession, the same stimuli were presented indifferent locations and with reversed Sþ/S−

functions. The number of discrimination re-versals was not preestablished but continueduntil fast acquisition of the reversed contingen-cies (as described in Phase 3) occurred.After fast acquisition of the reversed contin-

gencies was demonstrated, the tests for func-tional class formation began. The test procedureand criterion for functional class formation werethe same as in Phase 4.

Results and Discussion

Simple Discrimination ReversalsFigure 1 shows the total number of trials

required to meet the reversal training criterionfor each Sþ/S− reversal in Phase 1 (with twostimuli), Phase 2 (with four stimuli), and Phase 3(with six stimuli). Where the total number oftrials to meet the acquisition criterion exceeded20, more than one session was conductedbetween reversals. Both monkeys requiredmore than one session to acquire the firstsimple discrimination (labeled as Reversal 1).Monkey M23 quickly tracked the first reversal,whereas M18 quickly tracked the final tworeversals of Phase 1.Across Phases 2 and 3, both monkeys

generally tracked more accurately each succes-sive reversal. Within-session accuracy also in-creased (data not shown). The dashed lines inFigure 1 show the accuracy level when theacquisition criterion of six consecutive correcttrials was reached in the first seven trialsfollowing a reversal (i.e., fast reversal acquisi-tion–see reversals 22 to 25 for M18 and reversals18, 22, and 23 for M23). In Phase 3, when threeS− stimuli were available, if the monkey madeone error and then performed six consecutivetrials with no errors, then the monkey’s perfor-mance shows that the discriminations werereversed for all of the stimuli within a set afterexperiencing the consequences of a singleincorrect choice. Such a rapid change suggestsfunctional class formation.

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Tests for Functional Class Formation (Phases4 & 5)

Formal tests for functional class formationafter a contingency reversal with four of the sixstimuli evaluated whether monkeys also reversediscrimination with the stimulus pair that wasnot presented during reversal training. Becausecorrect choices were reinforced on test trials,the first choice made between the reintroducedstimuli is the appropriate measure of functionalclass formation. Both monkeys showed 100%accuracy in choosing between the reintroducedstimuli across all six tests conducted in Phase 4.During these sessions, the only error was made

by M18 and this did not involve a reintroducedstimulus.

In Phase 5, we introduced variations instimulus location and removed the class- specificreinforcement procedure. Figure 2 shows thetotal number of trials required to reach theacquisition criterion of six successive correcttrials following each reversal. Monkeys M18 andM23 completed 26 and 38 reversals, respectively;each was mastered in a single session. As before,the dashed lines in Figure 2 show the accuracylevels of fast reversal acquisition. M18 demon-strated fast reversal acquisition following rever-sals 11 and 25, whereas M23 did this followingreversal 32. Performance at the start of Phase 5

Fig. 1. Total number of trials per reversal in Phases 1, 2, and 3 for both M18 (upper graph) and M23 (bottom graph)during repeated reversals of simple discrimination training. Dashed lines, placed at the level of seven total trials, show whenthe acquisition criterion (six successive correct trials) was reached in seven trials (fast acquisition).

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was a bit less accurate than performanceat the end of Phases 3 and 4. This suggeststhat the removal of the class-specific reinforce-ment procedure and variation of stimuluspositions had little impact on performance.That being said, fast reversal acquisition wasless frequent in Phase 5 than at the end ofPhase 3. For this reason, more reversals wereconducted before testing for functional classformation.As in Phase 4, when testing for functional class

formation in Phase 5 the critical measure is thechoice between the Sþ and S− stimuli that werewithheld during reversal training. M18 alwayschose the correct previously withheld Sþ stimu-lus in all six tests of Phase 5. M23 chose thecorrect Sþ stimulus in five of six tests, with theerror occurring on the first test trial of the third

test (B1þ/B2−). The chance-level probability ofchoosing the correct of the two newly reintro-duced stimuli on any given trial was .5 and,therefore, the probability of correctly selectingthe Sþ on all six tests by chance was .03. Thus,our finding meets conventional alpha levelsused with inferential statistics. These dataprovide strong evidence of functional classformation.Overall performance accuracy for M18 and

M23 was 92.30% (36/39) and 86% (38/44),respectively, considering all test trials over thesix test sessions. Such data show that respondingwas accurate and stable with both baseline (i.e.,stimuli with functions reversed directly intraining) and test stimuli.As described above, the data reported for

Phase 4 left two questions unanswered. First, was

Fig. 2. Total number of trials per reversal during repeated reversals of simple discrimination training with 6 stimuli forbothM18 (upper graph) andM23 (bottomgraph) in Phase 5. Dashed lines, placed at the level of seven total trials, show whenthe acquisition criterion (six successive correct trials) was reached in seven trials (fast acquisition).

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the unchanged stimulus location a critical factorin functional class formation? Second, wasresponding based on discriminative control bythe reinforcer presented on a previous trial?The results of Phase 5 indicate that functionalclass formation was reliant on neitherprocedure.

In the present study, we investigated classformation in capuchinmonkeys (Cebus cf. apella)in the context of foraging tasks. The resultsdemonstrate the ability of primates to exhibitclass formation. The implications of theseresults are relevant to furthering the under-standing of complex learning mechanisms byanimals in nature, because class formation hasonly been documented in pigeons (Vaughan,1988) and sea lions (Kastak et al., 2001).

The number of experimental sessions re-quired to reach acquisition criterion was lessthan in previous studies that have demonstratedfunctional class formation with nonhumans.Each pigeon in Vaughan’s (1988) study wasgiven approximately 800 training sessions(64,000 trials) before evidence of class forma-tion was found. Each of Kastak et al.’s (2001) sealions was given an average of 160 trainingsessions (6,400 trials). In the present study,combining Phases 1 to 4, functional classformation was demonstrated after 40 trainingsessions (547 trials) forM18 and 39 sessions (564trials) for M23. In Phase 5, M18 was given 38training sessions (486 trials), and M23 was given48 training sessions (579 trials). Such dataillustrate that the procedure used in the presentstudy with capuchin monkeys produced hightraining efficiency. Other studies on functionalclass formation in our laboratory with the samespecies did not find the same results withcomputer-based training tasks (Goulart et al.,2003; Barros et al., in press). Nevertheless, thenoted differences between pigeons, sea lions,and monkeys may be more related to species–procedure interactions rather than the foragingprocedure per se (in other words, this proce-dure may not be as efficient with sea lions, forexample).

Although the data reported here do notsupport any discussion of intersubject variability,given the small number of subjects, furtherresearch should investigate the contribution ofreversal training, in the context of foragingtasks, toward reducing such variability. Indeed,the task described here may have takenadvantage of the natural skills of the monkeys

(i.e., foraging and locomotion), enhancing thecoherence between planned performance andperformance that actually occurred. That wouldconfirm the assumptions of Dube and McIlvane(1996) and McIlvane and Dube (2003) on thelack of procedural adequacy in research oncomplex stimulus control with nonhumansubjects.

The results reported here also seem toconfirm Sidman’s (2000) argument that theuse of class-specific reinforcers may facilitateclass formation. The Kastak et al. (2001) dataalso suggest there are benefits to using differen-tial outcomes.

One challenge to the use of the presentprocedure is the lack of automation (as inKastak et al., 2001). In some situations, this mayresult in some variability in the components ofthe procedure, such as the ITI and othertemporal components. Nevertheless, the proce-dure was designed in such way that it would befree from choice-biasing effects of the lack ofautomation (e.g., experimenter putting hisbaited hand into every box before moving theapparatus toward the monkey).

A better understanding of the role ofprocedural variables in the production ofcomplex behavior, such as functional classformation, in nonhuman subjects may inspirefurther research on methodological variablesthat may contribute to the development ofefficient procedures in basic research or even inthe treatment of people with severely delayeddevelopment (McIlvane, Dube, Serna, Lionello-DeNolf, Barros & Galvão, 2011).

In general, simple discrimination trainingprocedures reported here are highly effectiveand quickly produced accurate perfor-mance in capuchin monkeys. A less arbitraryprocedure that features ecologically relevantcomponents may have contributed to the fastacquisition of repeated reversals of simplediscriminations and consequent class forma-tion. We propose that future studies systemati-cally investigate this assumption of ecologicalrelevance.

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Received: June 28, 2012Final Acceptance: March 16, 2013

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