Analogical reasoning in baboons (Papio papio): Flexible reencoding of the source relation depending on the target relation
Analogical reasoning is a cornerstone of human cognition, but the extent and limits of analogical reasoning in animals remains unclear. Recent studies have demonstrated that apes and monkeys can match relations with relations, suggesting that these species have the basic abilities for analogical reasoning. However, analogical reasoning in humans entails two additional cognitive processes that remain unexplored in animals. These include the ability to (1) flexibly reencode the relations instantiated by the source domain as a function of the relational properties of the target domain, and (2) to match relations across different stimulus dimensions. Using a two-dimensional relational matching-to-sample task, the present study demonstrates that these two abilities are in the scope of baboons, given appropriate training. These findings unveil the richness of the cognitive processes implicated during analogical reasoning in nonhuman primates and further reduce the apparent gap between animal and human cognition.
KeywordsComparative cognition Categorization Cognitive flexibility Nonhuman primate
Analogical reasoning is a cornerstone of human thought (Sternberg, 1977). It is fundamental for a diversity of cognitive processes of considerable importance, such as classification (Ramscar & Pain, 1996), transfer of learning in new contexts (Gentner, Loewenstein, & Thompson, 2003), problem solving (Gick & Holyoak, 1980), and creative thinking (Holyoak & Thagard, 1996). Analogical thinking requires an ability to associate a relation instantiated by a first set of stimuli (source domain) to another relation shown by a second set of stimuli (target domain) (Gentner, 2002). Consider, for instance, the following analogy: Fish is to water as bird is to air. Understanding this analogy requires that the listener identify the relational similarity between the elements of the source domain (fish and water) and determine that the same relation exists between the elements of the target domain (bird and air). The ability to solve analogy problems is promoted during childhood by the acquisition of relational language (Gentner, Simms, & Flusberg, 2009; Loewenstein & Gentner, 2005). However, it remains unclear whether language learning acts as a booster that shifts attention toward the relational structure of a problem, or is simply a mandatory prerequisite for the appropriate encoding of analogy problems. Studies on analogy making in animals are perfect means to assess this issue of great theoretical importance.
Analogical reasoning has mostly been studied in animals with the relational matching-to-sample (RMTS) task (but see Haun & Call, 2009; Hribar, Haun, & Call, 2011; Kennedy & Fragaszy, 2008). In this task, the subject first perceives a set of stimuli (source domain) that are all the same (same relation) or all different (different relation), and then perceives two new sets of stimuli. One of the latter two sets (the target set) shows the same (same or different) relation as the source set, and the other shows the alternative relation. The animal is rewarded for choosing the comparison pair showing the same relation as the sample pair. A historical perspective on the use of the RMTS task pinpoints the pioneering contribution of Premack (1983), who reported that a language-trained chimpanzee (named Sarah) could solve the RMTS task. According to Premack, that success indicates that linguistic encoding is required for successful appreciation of second-order relations (i.e., relations between relations). Indeed, numerous studies following this first demonstration have failed to reveal RMTS abilities in language-naïve apes and monkeys (e.g., Flemming, Beran, & Washburn, 2007; Oden, Thompson, & Premack, 1988, 1990; Premack, 1983), with the notable exception of Thompson, Oden, and Boysen (1997), who reported that training to associate tokens to relations permits relational matching in language-naïve chimpanzees. However, this theoretical perspective on the contribution of language to successful RMTS has been challenged in light of a new set of experimental findings. Thus, a first set of studies showed that baboons (Fagot, Wasserman, & Young, 2001), and then pigeons (Cook & Wasserman, 2007), can solve this task when the relations are illustrated by arrays of multiple stimuli rather than by pairs of items. In addition, recent studies have revealed that nonhuman primates can pass the RMTS task with pairs of items rather than arrays after extensive training on the task (in a capuchin, Truppa, Mortari, Garofoli, Privitera, & Visalberghi, 2011; in baboons, Fagot & Parron, 2010; Fagot & Thompson, 2011) or with specific reinforcement contingencies (Flemming, Thompson, Beran, & Washburn, 2011). Vonk (2003) further reported relational matching in a gorilla and orangutans with limited training. These findings demonstrate some abilities to process second-order relations, and this is arguably a phylogenetic basis of analogical reasoning.
The demonstration that animals can match relations with relations is a very important first step in the assessment of analogy making in the species considered. However, analogical reasoning implies cognitive processes that are not restricted to the ability to match relations with relations. One important component of analogical reasoning in humans is that the encoding of the source domain often depends on the properties of the target domain (Holyoak & Thagard, 1989). Imagine an analogy task in which the source domain contains the “bee–hive” pair of items. Various relations exist between a bee and a hive, such as that the bee “lives in” or “works in” the hive. In that case, the relation to be processed must be specified by the relational properties of the target items. Thus the relation “works in” is highlighted when the target domain contains the “secretary–office” pair, but the relation “lives in” becomes salient when the target domain comprises the “human–house” pair.
Previous RMTS tasks used with animals have only manipulated a single stimulus dimension at a time, such as the shape (e.g., Fagot & Thompson, 2011; Truppa et al., 2011) or color (e.g., Fagot & Parron, 2010) of the stimuli. With these procedures, inspection of the source stimuli provided all the cues necessary to determine the (same or different) relation to be processed, with no need to reencode the source domain in terms of the properties of the target domain. This aspect of the task is at odds with analogy making in humans, in which the source domain is reencoded after the items of the target domain have been processed (Gitomer, Curtis, Glaser, & Lensky, 1987; Yan, Forbus, & Gentner, 2003). The strategy implying a reencoding of the source domain is of a higher level of complexity. It requires that the subject select the appropriate relation among a set of possible ones, and further imposes working memory constraints that are absent in the RMTS tasks previously employed with animals.
A second important feature of analogical reasoning in humans is the capacity to match relations instantiated by very different means. Consider, for instance, the “identity” relation: Two objects might be considered identical because they have the same color (e.g., tomato, fire truck), the same shape (moon, ball), or the same function (train, plane). Humans would have no real difficulty associating these pairs during an analogy task, because the items within each pair have something in common, independent of the dimension (shape, color, or function) shared by these items. Unfortunately, that ability to match relations across dimensions cannot be tackled by the version of RMTS procedure used so far with animals, again because these tasks only imply the processing of a single dimension at a time (e.g., the shape dimension, Fagot & Thompson, 2011; Truppa et al., 2011; or the color dimension, Fagot & Parron, 2010). Empirical data are needed in this domain to evaluate the power and flexibility of analogical thinking in animals.
We present below two experiments on baboons suggesting for the first time that an animal species can flexibly reencode the relations instantiated by the source domain as a function of the relational properties of the target domain (Exp. 1) and can, moreover, solve analogy problems involving the matching of relations instantiated by different stimulus dimensions (Exp. 2).
Experiment 1: Reencoding of the source relation depending on the target relation
In Experiment 1, we tested the ability of baboons to flexibly reencode the source domain as a function of the relational properties of the target domain. Baboons were trained and tested with a new version of the RMTS task in which the color and the shape of the source items were manipulated independently. In this task, the relevant (shape or color) dimension to process was only indicated by the properties of the target (comparison) pairs, which appeared after the sample had disappeared, therefore imposing a reencoding of the relational properties of the source pair—stored in working memory—after the target pairs have been processed.
Subjects and apparatus
The subjects were four male Guinea baboons (Papio papio; age range 4–7.6 years) previously trained in the RMTS task using pairs of monochromatic shapes as stimuli (Fagot & Thompson, 2011). They lived in a social group of 30 individuals within a 700-m2 enclosure and had free access to ten operant-conditioning test chambers, each equipped with a 19-in. touch screen, a food dispenser, and a radio frequency identification (RFID) reader that identified each baboon via a microchip implanted in each arm (Fagot & Bonté, 2010; Fagot & Paleressompoulle, 2009). A test program written with E-Prime Version 2 professional used the subjects’ identity to determine its “last stopping point” in the sequence of trial presentations, and assigned the independent variables to be experienced by each subject during the trial.
The source and target pairs were drawn from two distinct sets of six colors and six shapes, precluding physical matching by either color or shape. The left/right locations of the target pair were counterbalanced within each block. Correct responses were reinforced by a drop of dry wheat, and incorrect responses gave rise to a green screen and a 3-s time-out. Solving this task required the animal to remember the relationships instantiated by the source pair and to reencode that pair a posteriori, once the relevant dimension has been indicated by the structure of the comparison pairs.
Training and testing
Numbers of training blocks performed by each subject as a function of block size (from 120- to 2-trial blocks) for each type of trial (color and shape), as well as total numbers of trials and the corresponding standard deviations (SDs) per subject and trial type
Results and discussion
Mean percentages correct obtained for each baboon during Test Phase 1 of Experiment 1, as a function of trial type (color or shape) and relational consistency across dimensions (consistent or inconsistent relations)
Experiment 2: Matching relations across dimensions
Humans are capable of matching relations across dimensions and can, for example, indicate that two red objects illustrate the relation of sameness (considering color cues), just as do two identical triangles (considering the shape cues). To our knowledge, this ability to match relations across dimensions has never been investigated in animals. In Experiment 2, the baboons received cross-dimensional relational trials and were requested to match stimulus pairs on the basis of relational cues expressed by different dimensions in the sample (e.g., color cue) and comparison (e.g., shape cue) pairs. It was reasoned that correct relational matching responses with this design would provide evidence that the baboons could match relations across dimensions.
Results and discussion
In Experiment 2, we assumed that the vertical rectangles would signal the need to process color relations, while two white shapes would signal the need to process the shapes cues, because in the design of Experiment 1 the subjects had been trained to do so. However, inspection of Fig. 5 suggests that an alternative strategy was possible in the case of the same trials. Consider, for instance, the upper left panel of Fig. 5. In these trials, the baboons might consider the shape of the sample items, and match the sample and comparison pairs according to shape cues, regardless of color variations. Alternatively, they might match these two pairs on color cues in the trial of the upper right panel of Fig. 5. However, this strategy would not be efficient in the case of the different trials (see the bottom two panels of Fig. 5). To further the exploration of cross-dimensional matching in baboons, we thus investigated whether the three baboons that were above chance on average in the probe trials (with same and different trials confounded) also showed above-chance performance when the analysis was restricted to the different trials. Above-chance performance in these trials was confirmed for CAUET (66.2 % correct, Bonferroni-corrected binomial test, p < .0025), but not for DAN (54 % correct) or VIVIEN (25 % correct). The results therefore indicate that one of the baboons at least could match relations across dimensions.
One important property of analogical reasoning in humans is the fact that the dimension to process in the source domain is often determined by the relational properties of the target domain. Analogical reasoning therefore implies flexibility in the encoding of the source domain. The first major contribution of our study has been to demonstrate that a nonhuman primate species can express this flexibility. This finding is clearly demonstrated in Experiment 1, in which DAN could use the information provided by the comparison pair to appropriately consider the relation expressed by the relevant dimension of the sample pairs. It moreover did so in the consistent as well as in the more difficult inconsistent trials, in addition to the random blocks of trials, ruling out the possible effect of proactive interference from the previous trials.
Early comparative studies have already shown that apes (Thompson et al., 1997; Vonk, 2003) and baboons (Fagot & Thompson, 2011; Truppa et al., 2011) can match relations with relations in the unidimensional RMTS task involving pairs of items, but these findings were subject to criticisms by Penn, Holyoak, and Povinelli (2008), who argued that the nonhuman primates might use estimates of the perceptual variability in the source and target domains, rather than relations per se. This hypothesis is clearly ruled out by the fact that DAN continued to provide same responses when the stimulus dimension to process within the source pair indicated a same relation but the dimension to reject in that pair indicated a different relation. The second major contribution of our study has been to reveal that, in contrast to Penn et al.’s position, baboons may use a more complex cognitive strategy to solve the RMTS task, and continued to match relations even when perceptual variability cues conflicted with the relational judgments.
The last major contribution of this study has been to provide the first evidence that a baboon can match relations across dimensions. We observed that three baboons were successful on average in Experiment 2, and that one of them continued to be successful when the analysis was restricted to the different trials, on which the relational strategy was the only one viable. Noticeably, however, the baboon (CAUET) that showed the strongest evidence of cross-dimensional matching in Experiment 2 was not the same baboon (i.e., DAN) who demonstrated the best performance in Experiment 1. This finding is not surprising, considering that the cognitive processes required by these two tasks are somewhat different. Experiment 1 implied that the baboons respond to the task by matching the sample and comparison pairs on the same dimension, while neglecting the interference of the alternative dimension. By contrast, Experiment 2 implied that the subject should make use of the relations expressed by both dimensions and compare and combine the information derived from these two dimensions for correct matching. Regardless of the identity of the most successful baboons in Experiments 1 and 2, our study demonstrates that these two tasks are solvable by baboons, suggesting that these animals have at least the basic abilities to reason about second-order relations and to solve analogy problems.
An abundant literature has indicated that analogical performance is improved in human infants by the acquisition of verbal labels (Rattermann & Gentner, 1998). The immediate theoretical implication of our study is that language learning is not a mandatory prerequisite for the appropriate encoding of analogical problems. We do not want to assert that the baboon is a nonhuman primate species particularly gifted for analogical reasoning. Admittedly, their success in the task could only be obtained after thousands of training trials, and this training was likely the key factor leading to successful RMTS. The main function of word learning might be to boost analogical reasoning by rapidly orienting the attention of the children toward the relational structure of a problem (Loewenstein & Gentner, 2005). That function was likely accomplished in our study by the extensive training during which the baboons learned to flexibly shift their attention from dimension to dimension and relation to relation.
In spite of the remarkable achievement reported here, an important difference remains between analogical reasoning in humans and animals: The ability to solve analogical reasoning RMTS problems has been demonstrated in animals only in tasks involving dimensions and relations on which they have already been trained (e.g., Fagot & Thompson, 2011; Truppa et al., 2011). This aspect of the comparative literature contrasts sharply with analogical reasoning in humans, which readily extends beyond particular test dimensions or domains of knowledge (e.g., Gentner, 2003). The next challenge for researchers will be to identify the source of that difference between humans and animals. We suspect that its source will be found in the interplay between word (or symbol) learning and attentional processes.
This research was funded by Grant No. ANR-2010-BLANC-1908-01 and an EC EUPRIMNET-II grant, as well as by support from the PACA regional council (Volet Exploratoire, 2008). It was conducted at the Rousset-sur-Arc Primate Center (CNRS-UPS846), France. The authors thank D. Paleressompoulle, J. C Marin, and all of the staff of the primate center for technical support. Caralyn Kemp is acknowledged for her help in revising an early version of the manuscript. Robert French is acknowledged for stimulating discussions that triggered that research.
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