In this study, we investigated the ability of a fish species, the guppy, to perform two inhibition motor tasks based on the presence of transparent obstacles between the subject and the goal. Our results indicate that guppies are capable of solving inhibition motor tasks and that their performance is fully comparable to that observed in warm-blooded vertebrates.

In the cylinder task (experiment 1), guppies had to reach a food reward by entering a transparent cylinder from the open lateral sides, rather than trying to approach the food directly. This task was similar to the one adopted in a large study testing 32 species of mammals and birds20 and thus allowed a direct comparison between guppies and other species. We found no substantial difference between the percentage of correct trials made by guppies, 58% (53% if we consider only the first 10 trials), and the average performance of the mammalian and avian species tested by MacLean and colleagues (63% correct trials; Fig. 2). When apes are not considered, the difference between guppies and warm-blooded species (58%) is even smaller. Also the individual guppy with lowest performance (38% correct trials) outperformed several mammalian and avian species.

In contrast with two recent studies on birds21,35, we did not find evidence of an increase in the number of correct trials due to training. The absence of change in performance across the 50 test trials also allows to exclude that our measure of inhibitory motor control was affected by the novelty associated with the replacement of the cylinder. Indeed, guppies and other fish species often explore small, armless novel objects introduced in their aquaria43,44 and this behaviour might potentially affect performance. It remains to be addressed whether response to novelty might partially explain inter-specific differences in studies with a reduced number of testing trials20,21. The time to solve the task had a small but significant decrease over the trials, which might indicate a small performance improvement due to learning21. However, it is likely that, using this protocol, learning mostly occurred in the training phase with the opaque cylinder.

There is evidence that inhibitory control performance might depend on the context and the value of the reward40,45. For example, humans show greater inhibitory control with food than with money reward40. Although the procedure of our cylinder task was as close as possible to that adopted for mammals and birds, heterotherms such as guppies may assign a different value to a food reward because of their different metabolic requirements. We controlled for this issue by performing a second experiment in which guppies had to detour a transparent barrier to reach a social reward. The overall performance of guppies in the barrier task tends to be lower than the performance of guppies in the cylinder task. This difference might be explained by the fact that, in the barrier task, during the initial days, the guppies had to learn to detour the barrier and handle the transparency simultaneously; conversely, in the cylinder task, these two phases were separated because the animals were initially trained using an opaque cylinder. Experiments on infants46, cotton top tamarins18 and three species of apes19 showed that subjects initially trained using an opaque barrier performed better than those exposed only to a transparent barrier. In line with this interpretation, at the beginning of the barrier experiment, the performance of guppies was rather poor, less than 20% correct trials. This agrees with a previous study that compared the behaviour of guppies with a transparent and a semi-transparent barrier in 5 test trials, finding reduced detour performance with the transparent barrier42. However, in the present study, after three days of experiments (roughly corresponding to the length of the training using the opaque cylinder in experiment 1), the guppies reached a performance very close to that of the cylinder task (50%). We should additionally consider that the barrier was perhaps more difficult to detour because it was larger than the cylinder and was C-shaped. In the light of these clarifications, the performance of the guppies appears similar for the two different types of reward, and thus this study does not support the hypothesis that the high performance of guppies in experiment 1 was the consequence of a reduced attractiveness of the food reward compared to warm-blooded vertebrates.

The clear increase in the guppies’ percentage of correct trials across testing days in the barrier task was accompanied by a marked decrease in the time taken to solve the task. Both improvements likely indicate that the guppies had learned to handle the transparent barrier. It is interesting to note that a similar improvement was observed in some species (cotton-top tamarins:18; orangutans, Pongo pygmaeus:19) but not in others (gorillas, Gorilla gorilla; bonobos, Pan paniscus; and chimpanzees, Pan troglodytes 19). These three latter species performed quite well in the cylinder task20, and it is still to be addressed whether the differential performance in the two tasks was due to methodological reasons as proposed for guppies.

Only one other study has directly investigated inhibitory performance of fish. Danisman et al.47 trained cleaner fish, Labroides dimidiatus, in a reverse reward contingency task: subjects had to select the smaller food item between two options to receive the larger food item as a reward. They found a poor performance of cleaner fish with none of the eight subjects being able to learn the task. Many other species did not succeed in learning to solve this task (e.g., chimpanzees:48; Japanese macaques, Macaca fuscata:49; cotton-top tamarins:9; black and brown lemurs, Eulemur fulvus and E. macaco 17). The difference between the study on cleaner fish and our study on guppies is likely due to the large difficulty of the reverse reward contingency task. To address this point, we need to gather more data on the performance of fish in other inhibitory control tasks. Among the others, it will be important to focus on tasks requiring self-control (i.e., the choice between alternatives with different values and different costs), because self-control is generally considered the most challenging aspect of inhibitory control36.

An efficient inhibitory control has been usually considered typical of humans and primates11,12, and it has been shown to positively correlate with brain size in a recent comparative study20. As guppy’s brain is more than 100 times smaller than the brain of the smallest species included in that comparative study, the performance of the guppies in the cylinder task is exceedingly higher than would be expected based on brain size. Together with other evidence21, this suggests that brain size alone cannot explain the large differences in inhibitory motor control observed among species.

In MacLean et al.’s study, the main predictor of inhibitory motor control performance was absolute brain size20. Perhaps this relationship only holds considering a sample of species with a limited range of body size or within a restricted taxonomic group. As recently discussed by Herculano-Houzel50, brain mass is only a proxy for the neuronal capability devoted to complex information processing. If larger bodies require larger brains to operate, then in larger species only part of the increase in brain mass can contribute to behavioural complexity. However, controlling for the whole brain allometry is unlikely to account for the performance of guppies, as fish have, on average, a relative brain weight ten times smaller than mammals and birds51.

Another important issue to be considered is that the brain of different species can differ in structure at different scale levels, and these differences are expected to increase with increased phylogenetic distance. For example, neural density is extremely variable both within mammals and between mammals and birds50. Recently, Kabadayi et al.21 found that in three corvid species, performance in a inhibitory motor control task was much higher than the average performance found in mammals, although their brain mass is much smaller. This result could partly be explained by the fact that the forebrain of several bird species contains many more neurons compared to that of mammals52. As another example, some insects are capable of exceptional cognitive performance despite having a brain that is extremely small even compared to a small fish like the guppy; it was suggested that this may be related to characteristics of the neural circuits that present wide differences between vertebrates and arthropods53.

Though they belong to the same clade, the modern ray-finned fishes (to which teleosts belong) diverged approximately 450 million years ago from the line of fish that gave origin to land vertebrates. In addition, a major genomic rearrangement – a whole-genome duplication – occurred in the line leading to teleosts soon after the separation; there is now evidence that this event produced a significant enrichment of the set of genes available for the evolution of novelties in the nervous system of this vertebrate group54. Therefore, the brains of teleost fish and land vertebrates evolved in large part independently and may show a very different anatomical and cytoarchitectonic structure. However, the cytoarchitectonic structure of the teleost brain and the localisation of the functions studied here are less well known compared to warm-blooded vertebrates and therefore any conclusion on this topic is premature.

A second important factor that can explain interspecific differences in cognitive abilities across all vertebrates is the selective pressure exerted by the environment in which a species evolved. Several ecological factors have been suggested to promote the evolution of inhibitory control. For example, species that typically feed on moving prey might show more impulsiveness11. Alternatively, species with a complex social environment may have been selected for greater inhibitory control, a hypothesis that has found some support20,55. Another possibility is that inhibitory control evolves as a by-product of selection on other behaviours and cognitive functions. As the capacity to inhibit prepotent but unfavourable responses is an important prerequisite for a wide range of cognitive tasks6,7,8,9,10, it is conceivable that selection acting on these cognitive functions can indirectly select for high inhibitory control.