Analogical reasoning is vital to advanced cognition and behavioral adaptation. Many theorists deem analogical thinking to be uniquely human and to be foundational to categorization, creative problem solving, and scientific discovery []. Comparative psychologists have long been interested in the species generality of analogical reasoning, but they initially found it difficult to obtain empirical support for such thinking in nonhuman animals (for pioneering efforts, see []). Researchers have since mustered considerable evidence and argument that relational matching-to-sample (RMTS) effectively captures the essence of analogy, in which the relevant logical arguments are presented visually []. In RMTS, choice of test pair BB would be correct if the sample pair were AA, whereas choice of test pair EF would be correct if the sample pair were CD. Critically, no items in the correct test pair physically match items in the sample pair, thus demanding that only relational sameness or differentness is available to support accurate choice responding. Initial evidence suggested that only humans and apes can successfully learn RMTS with pairs of sample and test items []; however, monkeys have subsequently done so []. Here, we report that crows too exhibit relational matching behavior. Even more importantly, crows spontaneously display relational responding without ever having been trained on RMTS; they had only been trained on identity matching-to-sample (IMTS). Such robust and uninstructed relational matching behavior represents the most convincing evidence yet of analogical reasoning in a nonprimate species, as apes alone [] have spontaneously exhibited RMTS behavior after only IMTS training.

Results and Discussion

13 Smirnova A.A.

Lazareva O.F.

Zorina Z.A. Use of number by crows: investigation by matching and oddity learning. 14 Katz J.S.

Wright A.A.

Bodily K.D. Issues in the comparative cognition of abstract-concept learning. Our findings come from three separate behavioral assessments that followed pretraining and pretesting on identity matching-to-sample (IMTS; see the Supplemental Experimental Procedures available online), deploying behavioral methods that were earlier used by Smirnova, Lazareva, and Zorina []. In that prior IMTS period, two hooded crows were shown several different kinds of visual stimuli: single stimuli of varying colors or shapes and clusters of stimuli containing varying numbers of items. The birds were taught to match stimuli by color, shape, and number of items, but not size. After learning these various IMTS tasks, the crows reliably transferred discriminative responding to new stimuli from the same categories that were used in training ( Table S2 ) as well as to stimuli from an altogether different category ( Figure S2 )—stimuli varying in size—suggesting that the birds had acquired a general rule that was based on physical identity [].

7 Vonk J. Gorilla ( Gorilla gorilla gorilla) and orangutan ( Pongo abelii) understanding of first- and second-order relations. Figure 1 Examples of Identity and Relational Trials across Eight Exemplary Trials for Size Stimuli Show full caption On three-fourths of the trials (1–3 and 5–7), the correct test stimulus was an identity match to the sample. On one-fourth of the trials (4 and 8, shaded gray), the correct test stimulus was a relational match to the sample. Figure 2 Examples of Identity and Relational Trials across Eight Exemplary Trials for Shape Stimuli Show full caption On three-fourths of the trials (1–3 and 5–7), the correct test stimulus was an identity match to the sample in shape. On one-fourth of the trials (4 and 8, shaded gray), the correct test stimulus was a relational match to the sample. Figure 3 Examples of Identity and Relational Trials across Eight Exemplary Trials for Color Stimuli Show full caption On three-fourths of the trials (1–3 and 5–7), the correct test stimulus was an identity match to the sample in color. On one-fourth of the trials (4 and 8, shaded gray), the correct test stimulus was a relational match to the sample. The key behavioral assessments followed, in which novel pairs of items served as the sample and test stimuli []. The visual dimensions in these assessments were size, shape, and color ( Figures 1 2 , and 3 show several illustrative, not actual, trial sequences). On identity trials, we arranged differential reinforcement (food was given only after correct choices) to promote continued discriminative responding; accurate choice responding here could be based on either physical or relational matches between the sample pair and the correct test pair. On the critical relational trials, we arranged nondifferential reinforcement (food was given after all choices) because we did not want to teach the crows the very behavior that we were assessing; accurate choice responding here could only be based on relational matches between the sample pair and the correct test pair. Assessment sessions were conducted 5 days a week and contained 48 trials: 36 identity trials and 12 relational trials. The sessions contained six blocks (each block containing six identity trials and two relational trials); the trial order was randomized within each of the six blocks. On all trials, we scored as “correct” those choices that accorded with relational matching. Each assessment phase lasted eight sessions.

The first assessment phase involved size. Figure 1 shows that on half of the trials the sample pair involved shapes of the same size, whereas on the other half of the trials the sample pair involved shapes of different sizes. With the different-sized sample and choice pairs, the large shape always appeared on the left and the small shape always appeared on the right in order to keep the number of sample-comparison combinations within manageable limits. The palette of simple black shapes from which the sample and test pairs could be selected contained a square, a rectangle, a circle, an oval, a wide triangle, and a narrow triangle. These shapes could be large or small; the overall area of the two test pairs was equated, so that this stimulus property could not control the crows’ behavior. Identity matching trials were arranged in which one test pair presented the same shapes in the same sizes as the sample pair; each of the sample and test pairs involved the same shape, and only correct choices were reinforced on these trials. Relational matching trials were arranged in which neither of the test pairs matched the sample pair in shape, thereby eliminating control by physical identity; on these trials, either correct or incorrect choices were reinforced.

The second assessment phase involved shape. Figure 2 shows that on half of the trials the sample pair involved identical shapes, whereas on the other half of the trials the sample pair involved nonidentical shapes. In this assessment phase and the next, the items in each pair were arranged along the positive diagonal in order for the spatial arrangement to differ from the horizontal arrangement in the prior assessment phase and to keep the number of sample-comparison combinations within manageable limits. The palette of shapes contained equal-sized circles, squares, triangles, and crosses that could be colored red, yellow, blue, or green. Identity matching trials were arranged in which one test pair presented the same shapes as the sample pair; only correct choices were reinforced on these trials. Relational matching trials were arranged in which neither of the test pairs matched the sample pair in shape or color, thereby eliminating control by physical identity; on these trials, either correct or incorrect choices were reinforced.

15 Håstad O.

Victorsson J.

Ödeen A. Differences in color vision make passerines less conspicuous in the eyes of their predators. The third assessment phase involved color (crows have excellent color vision []). Figure 3 shows that on half of the trials the sample pair involved identical colors, whereas on the other half of the trials the sample pair involved nonidentical colors. The palette of colors contained equal-sized circles, squares, triangles, and crosses that could be shown in red, yellow, blue, or green. Identity matching trials were arranged in which one test pair presented the same colors as the sample pair; only correct choices were reinforced on these trials. Relational matching trials were arranged in which neither of the test pairs matched the sample pair in color or shape, thereby eliminating control by physical identity; on these trials, either correct or incorrect choices were reinforced.

In the size-assessment phase, 60 combinations of stimuli were used as samples on relational trials (they were never repeated within sessions and were presented a maximum of two times, in different locations, across sessions) and 12 combinations of stimuli were used as samples on identity trials (they were never repeated within sessions and were presented a maximum of 24 times across sessions). In the shape and color assessment phases, trial-unique combinations of stimuli were used as samples on all relational and identity trials.

2(1) = 0.94, p = 0.33; crow 2: χ2(1) = 1.57, p = 0.21] and no interactions of Session with the other variables (daily accuracy scores are reported in Table 1 Mean Percentage of Correct Choices by Crows 1 and 2 Dimension Trial Type Session 1 Sessions 1–8 Crow 1 Size Identity 77.78 79.51 relational 75.00 72.92 Shape identity 75.00 70.83 relational 91.67 73.96 Color identity 66.67 76.04 relational 58.33 61.46 Crow 2 Size identity 75.00 76.39 relational 91.67 76.04 Shape identity 63.89 71.18 relational 75.00 77.08 Color identity 77.78 78.82 relational 75.00 71.88 Accuracy scores are from identity (IMTS) and relational (RMTS) trials on all three dimensions in session 1 and across sessions 1–8. See also Table S1 Throughout all three assessment phases, the crows exhibited highly accurate choice responding on both identity and relational trials (fourth column in Table 1 ). We individually assessed each crow’s behavior with a logistic regression examining trial type, stimulus dimension, and session. These regression analyses revealed no significant changes in choice accuracy over the eight sessions in each phase [crow 1: χ(1) = 0.94, p = 0.33; crow 2: χ(1) = 1.57, p = 0.21] and no interactions of Session with the other variables (daily accuracy scores are reported in Table S1 , and details of the statistical analyses are reported in the Supplemental Experimental Procedures ); therefore, subsequent discussion does not consider this factor.

We next compared accuracy scores on the different kinds of trials against 50% (representing random choice between the test pairs). Averaged across all eight sessions, crow 1 responded at significantly above chance accuracy levels to all six different kinds of stimuli (B = 1.06, SE = 0.068, Z = 15.57, p < 0.0001), with accuracy ranging from 61.46% to 79.51% correct. There was a significant main effect of trial type [χ2(1) = 3.99, p = 0.0457], with slightly lower accuracy on relational trials (69.44%) than on identity trials (75.46%). There was also a marginally significant trial type × stimulus dimension interaction [χ2(2) = 5.67, p = 0.059]. Follow-up tests within each stimulus dimension disclosed that the interaction was due to a significant effect of trial type for the color dimension (B = −0.68, SE = 0.25, Z = 2.74, p = 0.0061), but not for the shape (B = 0.18, SE = 0.27, Z = 0.68, p = 0.49) or size dimensions (B = −0.36, SE = 0.27, Z = 1.33, p = 0.183), suggesting that accuracy on color relational trials was a bit poorer than on the remaining kinds of trials. Averaged across all eight sessions, crow 2 responded at significantly above chance accuracy levels to all six different kinds of stimuli (B = 1.13, SE = 0.067, Z = 16.34, p < 0.0001). Accuracy ranged from 71.18% to 78.82% correct, with accuracy being numerically (but not reliably) lower on identity trials (72.22%) than on relational trials (80.56%). The logistic regression yielded no other significant effects.

Because of the importance of spontaneity to interpreting the crows’ relational matching-to-sample (RMTS) behavior, we also analyzed choice behavior in session 1 of each assessment phase (third column in Table 1 ) using a similar logistic regression as in the prior analyses. In session 1, crow 1 responded at significantly above chance levels of accuracy (B = 1.08, SE = 0.20, Z = 5.39, p < 0.0001), but there were no significant effects of trial type or stimulus dimension; summed across all three dimensions, accuracy on identity trials averaged 73.15% correct, and accuracy on relational trials averaged 75.00% correct. Crow 2 also responded at significantly above chance accuracy levels in session 1 (B = 1.11, SE = 0.20, Z = 5.53, p < 0.0001), but there were no significant effects of trial type or stimulus dimension; summed across all three dimensions, accuracy on identity trials averaged 72.22% correct, and accuracy on relational trials averaged 80.56% correct.

We thus found that, when tested during the size-assessment phase immediately after initial IMTS training, our crows not only responded discriminatively on identity matching trials, but also did so on relational matching trials, all of these trials for the first time involving two-item sample and test stimuli. These results represent striking behavioral evidence that the crows spontaneously perceived the relation between relations without ever having been explicitly trained to do so.

That initial size assessment entailed sample and comparison stimuli that were horizontally ordered large (left) to small (right) with different-sized pairs. Could that incidental spatial cue have affected the accuracy of the crows’ later choice behavior? Evidently not. The crows continued to respond at similarly high levels of accuracy on identity and relational trials during the shape and color assessment phases, during which the items in the sample and comparison pairs were diagonally arranged.

This documentation of RMTS behavior is particularly noteworthy because our crows exhibited discriminative relational matching (averaging 77.78% correct) that was just as robust as their identity matching (averaging 72.69%) in session 1 across all three assessment phases. Although physical identity could have guided the crows’ choice behavior on IMTS trials, physical identity could not have done so on RMTS trials, as no physical matches were possible between the sample pairs and the correct test pairs. These results perhaps surprisingly suggest that physical identity contributed little or nothing to our crows’ testing performance; relational processing seems to have been of prime importance to controlling the birds’ choice behavior.

Our results thus constitute unprecedented behavioral evidence of analogical reasoning by a nonprimate animal. They therefore add to growing research undermining the influential claims of such famous philosophers as René Descartes and John Locke that only humans are capable of abstract thought. Relational reasoning—particularly appreciating the relation between relations, as in analogies—can no longer be deemed to be the unique pinnacle of human cognition.

16 Emery N.J. Cognitive ornithology: the evolution of avian intelligence. 17 Portmann A. Études sur la cérébralisation chez les oiseaux. II. Les indices intracérébraux. 18 Güntürkün O. The convergent evolution of neural substrates for cognition. It may be no accident that crows performed so impressively in our study; they stand out among birds in their highly developed neuroanatomy []. More generally, mounting evidence indicates that although birds do not have a brain structure that is homologous to the mammalian prefrontal cortex, the avian nidopallium caudolaterale may effectively mediate complex cognitive functions, perhaps representing a case of convergent evolution [].

19 Truppa V.

Piano Mortari E.

Garofoli D.

Privitera S.

Visalberghi E. Same/different concept learning by capuchin monkeys in matching-to-sample tasks. 20 Wasserman E.A. Development and evolution of cognition: one doth not fly into flying!. It should nevertheless be appreciated that we are not claiming that our crows’ spontaneous relational matching behavior arose entirely de novo. Indeed, we believe that their earlier IMTS training is likely to have enabled them to grasp a broadly applicable concept of sameness that could apply to novel two-item sample and test stimuli involving only relational sameness []. Just how that remarkable transfer is accomplished represents an intriguing matter for future study. Nor are we claiming that crows will prove to be the only nonprimate animals that are capable of exhibiting such spontaneous relational matching behavior. Future research must be undertaken in which different species are given comparable pretraining experience to our crows. Until such systematic comparative research is conducted, it would be premature to offer speculative evolutionary accounts as to why crows appear to have excelled in solving this challenging cognitive task. It would also be premature to suggest that simply because crows successfully master RMTS tasks, they process the stimuli and relations in the same way as do humans and other nonhuman animals.