Inhibitory control is a core component of executive functions, and can be defined as inhibiting prepotent responses in favor of more appropriate and productive actions for a given situation (Casey et al., 2011; Diamond, 2013). Motor self-regulation, which requires stopping a prepotent but counter-productive movement (Beran, 2015), is an essential aspect of inhibitory control. It is thought to underpin more taxing inhibitory processes, as they cannot be expressed if such basic self-regulation is weak. Given its importance, comparative investigations of motor self-regulation generate insights into aspects of cognitive evolution, such as whether this skill correlates with more complex cognition and ecological and phylogenetic factors (MacLean et al., 2014; Meier et al., 2017).

Recent years have seen several comparative investigations of motor self-regulation on a wide range of species, using detour tasks around transparent barriers (Amici et al., 2008; Vlamings et al., 2010; MacLean et al., 2014; Kabadayi et al., 2016). In order to reach for the visible reward behind the barrier, the subject must inhibit the prepotent motor response of directly reaching for the reward, and instead detour around the barrier (Diamond, 1990). While such comparisons may reflect different degrees of motor self-regulation abilities across taxa, the comparisons are often based on the average scores of adult individuals over few trials, and do not inform how the skill develops in different lineages.

Extending the comparisons to the developmental patterns may reveal important clues to cognitive evolution. Species differences in mature characters often result from alterations in developmental pathways (Gould, 2002; West-Eberhard, 2003; Rosati et al., 2014); thus, comparing the pace and pattern of cognitive development between species may explain variation in mature cognition. Although both comparative and developmental studies have long pedigrees, they are rarely integrated, and important insights may be overlooked (Gomez, 2005; Rosati et al., 2014). For example, inhibitory control develops more slowly in bonobos than chimpanzees, which may explain why adult chimpanzees display higher levels of self-control compared to bonobos (Rosati et al., 2007, 2014; Herrmann et al., 2010; Wobber et al., 2010).

Motor self-regulation tasks requiring detours around barriers have rarely been used in developmental studies. Human infants show a clear developmental progression between 6 and 12 months in reaching around transparent barriers (Diamond and Gilbert, 1989). Initially they find it difficult to reach through the side opening of a transparent box and instead attempt to directly reach for the visible but blocked reward. They gradually overcome this difficulty and execute detours around transparent barriers by the end of their first year (Diamond, 1990). Rhesus macaques (Macaca mulatta) go through a similar developmental trajectory between 1 and 4 months (Diamond and Goldman-Rakic, 1986). At a certain point in development, once they have attained object permanence (Piaget, 1954), both humans and rhesus macaques are proficient in detouring opaque barriers while they experience problems in detours around identical but transparent barriers, likely because the visible reward creates a strong motivational pull for a direct reach (Lockman, 1984; Diamond, 1991). Thus, the improvement in detour performance around transparent barriers is attributable to the development of motor self-regulation skills (Diamond, 1990).

There are currently no developmental studies on motor self-regulation involving detours in birds. Ravens (Corvus corax) are good candidates for such developmental investigation because they excel at inhibition tasks as adults, and are paralleled only by chimpanzees in a motor self-regulation task involving detours around transparent barriers (Kabadayi et al., 2016). Ravens are also renowned for their cognitive skills in various domains (Güntürkün and Bugnyar, 2016), including self-control (Dufour et al., 2012), and complex planning (Kabadayi and Osvath, 2017), often matching great apes in their abilities. Thus, investigating the development of motor self-regulation in ravens might reveal developmental patterns similar to those in other cognitively proficient mammals (Diamond, 1990; Rosati et al., 2014). This in turn can have implications for the understanding of independent evolution of complex cognition, i.e., whether different lineages – such as corvids and primates – undergo similar developmental stages when building complex cognition (Osvath et al., 2014).

We tested the development of motor self-regulation in raven chicks using two detour tasks: the transparent cylinder task and the mesh barrier task (Figure 1). The transparent cylinder task has recently become a benchmark test for motor self-regulation and has been administered to a wide range of species, including adult ravens (MacLean et al., 2014; Kabadayi et al., 2016). It is functionally identical to the object-retrieval task, which has been used in previous developmental studies in human and rhesus macaque infants (Diamond, 1990). The mesh barrier task, which has a long history within comparative psychology, was modeled after previous studies that used grid or wire barriers to study detour behaviors (Köhler, 1927).

In the transparent cylinder task, a reward is placed at the center of a transparent cylinder with two openings at its ends. The subject must inhibit the response of directly reaching for the visible but blocked reward and instead detour through either of the two openings in the ends of the cylinder. An opaque cylinder is used as a control. Opaque controls have also been used in functionally similar tasks in previous developmental studies on human and rhesus macaque infants (Diamond, 1990). Because the opaque and transparent cylinder differ only in reward visibility, and require identical detours to obtain the reward, a lower performance on the transparent task compared to the opaque task reflects the difficulty to motor self-regulate. It is then likely that the visibility of the reward creates a prepotent tendency to directly reach for it.

The mesh barrier task, used in this study, consists of a grid barrier that required the animal to walk around the barrier in order to obtain the reward. Since the mesh barrier partly occludes the reward by its wires, it is arguably less taxing than the transparent cylinder where the whole reward is clearly visible, and many species execute more efficient detours around mesh barriers than transparent ones (Regolin et al., 1994; Lockman and Adams, 2001; Vallortigara and Regolin, 2002; Juszczak and Miller, 2016). The cylinder task, with its transparent surface, is likely also more artificial than the mesh barrier task, in the sense that complete transparency is an unusual property of the environment. Whereas the animal might early on learn that it cannot walk through opaque objects even if it sees the goal, it might require specific experiences with transparent surfaces to understand the affordances of such materials.

Therefore, we predicted the ravens’ motor self-regulatory development would be reflected in their performances on these tasks: they will perform better and succeed earlier on the mesh barrier task compared to the transparent cylinder task, and they will perform most accurately on the opaque cylinder task as the invisible reward behind the opaque barrier creates no motor self-regulation challenges. Detouring around the opaque barrier instead requires object permanence as it involves orienting toward an object out of sight. Ravens become successful in searching and retrieving fully hidden objects (object permanence) around 8 weeks of age (Bugnyar et al., 2007). Thus, we predicted they would succeed in detouring around the opaque barrier around this time. However, we started the tests as soon as the ravens fledged (on their 6th week), in order to capture a wider possible period of motor self-regulation development.

On average, the four ravens first reached 100% performance in the opaque cylinder task in week 7.5 (minimum: 7, maximum: 8); the mesh barrier task in week 7.5 (minimum: 6, maximum: 9); and the transparent cylinder task in week 9.75 (minimum: 9, maximum: 10). The weekly development of the performance on the two motor self-regulation tasks and the opaque cylinder task is shown in Figure 2. Regression analyses revealed that the motor self-regulatory responses in both tasks increased significantly over weeks (transparent cylinder task: EST = 1.36, SE = 0.21, z = 6.65, p < 0.001, mesh barrier task: EST = 1.35, SE = 0.28, z = 4.76, p < 0.001). The performance levels in the opaque cylinder also improved significantly over weeks (EST = 2.42, SE = 0.48, z = 5.00, p < 0.001). In the first week of testing, performance levels in the transparent cylinder were significantly worse than the opaque cylinder (EST = -1.81, SE = 0.49, z = -3.70, p < 0.001) and the mesh barrier (EST = -1.66, SE = 0.47, z = -3.54, p < 0.001).

The performances in the transparent cylinder increased less steeply over time compared to the opaque cylinder (EST = -1.054, SE = 0.48, z = -2.17, p = 0.029), but there was no significant difference between the performance slopes on the transparent cylinder and mesh barrier (EST = -0.012, SE = 0.29, z = -0.043, p = 0.966). Performance levels in the opaque cylinder were higher than in the transparent cylinder in the same week (except for the male in week 7 and until the ravens reached ceiling performance in both tasks). There was greater individual variation in the mesh barrier as every individual reached the criterion on different weeks (weeks 6, 7, 8, and 9, respectively). The bird that succeeded earliest on the mesh barrier (week 6) did not succeed earlier than the other birds on the transparent cylinder. All birds succeeded on the mesh barrier before the transparent cylinder. One individual succeeded on the mesh barrier a week before the opaque cylinder. For all three tasks, once the subjects reached 100% performance on a given week, their performance on the same task always remained 100% in the following week, after which the testing ended. By week 10, all four birds succeeded in all tasks.

Because all four birds succeeded on all three detour tasks latest at 10 weeks, we started testing a naïve chick with all three tasks when she was 10 weeks old (Unfortunately, only one chick was available). Her performance on the mesh barrier and the opaque cylinder was 100% already on the first week of testing, and remained 100% on the subsequent week of testing. She reached 100% on the transparent cylinder in the third week of testing – when she was 12-weeks old – with a first week performance of 3 out of 10, and a second week performance of 5 out of 10. Her performance remained 100% on the subsequent week (week 13).

As predicted, greater reward visibility posed a bigger challenge to the ravens, as reflected in the order in which they succeeded on the tasks. At an earlier developmental stage, the ravens performed worse on the transparent barrier than the mesh barrier. This difference was probably due to the stronger perceptual pull by the more visible reward behind the transparent barrier. Similarly, the successes on the transparent cylinder were initially fewer than those on the opaque cylinder. When the ravens were successful in retrieving the reward from the opaque cylinder, they had difficulty executing the same behavior on the transparent cylinder for the next few weeks. Thus, the gradual increase in performance in the transparent cylinder task can be attributed to the development of motor self-regulation.

Similar developmental patterns using transparent and opaque barriers have been found in human infants between 6 and 12 months and rhesus macaque infants between 1 and 4 months (Lockman, 1984; Diamond, 1990; Lockman and Adams, 2001). During these months, both human and rhesus macaque infants have difficulties in making detours around a transparent barrier while they are proficient on opaque barriers. Thus, the developmental pattern of motor self-regulation in ravens resembles that of children and rhesus macaques, albeit the rate is considerably accelerated in absolute time. Our results also support previous findings of that reduced reward visibility improves detour performance (human infants: Lockman and Adams, 2001; Noland, 2008; chickens: Regolin et al., 1994; mice: Juszczak and Miller, 2016; dogs: Chapuis et al., 1983; cats: Poucet et al., 1983). Ravens succeeded in detouring around the opaque barrier around 8-week post-hatch, which coincides with the time they achieve object permanence skills (uncovering a fully hidden object; Bugnyar et al., 2007). This developmental pattern is also found in human infants, albeit at a later age (Lockman, 1984). However, there are possibly some task differences between species: ravens had to move their whole body to obtain the reward, but the primates could reach for the reward behind the barrier using their hands only while sitting in front of the barrier (Diamond, 1990).

Improvement on detour tasks across trials is a common finding in many species, even in adults; indeed, detour problems have been used to study various learning processes (Wyrwicka, 1959; Scholes and Wheaton, 1966; Boogert et al., 2011; Vernouillet et al., 2016). However, the results in this study likely do not reflect merely a task learning phenomenon decoupled from a developmental one. For example, the 10-week old raven that was tested for the first time immediately performed flawlessly on the mesh barrier task. That this bird did not need any specific experience with the materials or tests to pass suggests that the improvement on the mesh barrier task for the other four birds reflected largely a developmental phenomenon. This bird might have had general experience from moving about outside the nest and encountering situations where it could not reach goals due to physical obstacles. The other birds had little such experience when they were tested the first time.

When it comes to the transparent cylinder task, the 10-week old bird that was tested for the first time did not reach the criterion immediately but needed some experience until she succeeded at 12 weeks post-fledging. This might be due to the fact that transparent objects are highly artificial and they pose conflicting visual-tactile information. Accordingly, it takes more experience to understand them as a barrier (Bojczyk and Corbetta, 2004). And yet, this individual was 100% correct on the transparent cylinder task already in her third week of testing. Her performance could of course also reflect slight variations in the speed of cognitive development between individuals. Among the other four birds that started the tests earlier, three individuals required 5 weeks and one individual required 4 weeks of testing until they reached 100%. This could suggest that the performance on the transparent cylinder increases faster when tests start at a later stage, possibly due to an interaction between experience and development.

Adult ravens, including one sub-adult (a 1-year-old), performed 100% correct on the transparent cylinder task without training, indicating that they do not need any specific training on the materials for succeeding (Kabadayi et al., 2016). The finding that untrained adult ravens perform perfectly on the transparent cylinder task suggest they already have a fully developed motor self-regulation ability in relation to detours by the age of one. Thus, the improvement of the raven chicks on the transparent cylinder task points to developmental maturation. However, it is well-known that repeated task exposure plays an important role in development – including detours around transparent barriers (Bojczyk and Corbetta, 2004). It is likely that birds with more experience with transparency succeed earlier than those without (as hinted at by the control bird). Consistent with this idea, human infants that were tested repeatedly throughout development (longitudinal group) succeeded in taking detours around transparent barriers about 2–4 weeks earlier than infants in the cross-sectional group that did not receive repeated trials (Diamond, 1988). Cognitive development always occurs in relation to an environment, so it is difficult to pinpoint the exact timings of different skills on a species level. Nonetheless, it is possible to find the earliest emergence of a particular skill when comparing subjects with different experiences. It is possible that the four ravens tested longitudinally showed the earliest possible onset of these skills as they were specifically provided the tasks early on.

Despite difficulties with demarcating learning from development – as learning is part of ontogeny – there are further reasons to think that a learning account decoupled from other cognitive maturation offers a less convincing explanation. The order in which the detour tasks were solved, based on increased reward visibility, is predicted from a gradual development of inhibitory skills. The motor self-regulation account is also consistent with the finding that ravens found it harder to make detours around transparent barriers while being proficient in detouring identical but opaque ones. Such an “opaque advantage” during a certain developmental period suggests a knowing/acting mismatch, which is common in other types of inhibition problems. That is, the animal knows the task rule (detour around the barrier) but cannot act on that rule, because the visible reward creates a strong incentive for a direct reach. The development of motor self-regulatory skills thus frees this knowledge, and detours can be executed by inhibiting motor responses instigated by the visible reward.

In summary, we found that ravens follow a developmental trajectory in motor self-regulation similar to that of primates, albeit at a considerably faster pace in absolute time. This higher speed is consistent with previous developmental studies on other cognitive skills in ravens, such as object permanence (Bugnyar et al., 2007) and gaze following (Schloegl et al., 2007). Given the vast phylogenetic separation between birds and mammals, the results may shed glimpses of light on the questions surrounding independent evolution of complex cognition. If cognitive skills are similar in adult ravens and apes, and if these skills appear to rely on similar developmental pathways, it might suggest that parallelism, instead of convergence, is the evolutionary mechanism (Osvath et al., 2014), however, it could also suggest that there is only one way to developmentally produce certain forms of cognition. As both task affordances and contextual factors might affect performance, future developmental studies should also include other motor self-regulation tasks – such as the stop-signal task – to gain a more detailed understanding of the development of motor self-regulation.

CK: study design, data collection, data analysis and interpretation, manuscript drafting. IJ: data analysis and interpretation, manuscript drafting. MO: study design, data interpretation, and manuscript drafting. All authors approved the final version to be published.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.