The insight that animals' cognitive abilities are linked to their evolutionary history, and hence their ecology, provides the framework for the comparative approach. Despite primates renowned dietary complexity and social cognition, including cooperative abilities, we here demonstrate that cleaner wrasse outperform three primate species, capuchin monkeys, chimpanzees and orang-utans, in a foraging task involving a choice between two actions, both of which yield identical immediate rewards, but only one of which yields an additional delayed reward. The foraging task decisions involve partner choice in cleaners: they must service visiting client reef fish before resident clients to access both; otherwise the former switch to a different cleaner. Wild caught adult, but not juvenile, cleaners learned to solve the task quickly and relearned the task when it was reversed. The majority of primates failed to perform above chance after 100 trials, which is in sharp contrast to previous studies showing that primates easily learn to choose an action that yields immediate double rewards compared to an alternative action. In conclusion, the adult cleaners' ability to choose a superior action with initially neutral consequences is likely due to repeated exposure in nature, which leads to specific learned optimal foraging decision rules.

to BJW. We thank the editor and two anonymous reviewers for comments that have improved the paper, Megan Luetje for recruiting our human participants, and Jeffrey Kirchner for his software programming.

Species vary in the ease with which they can solve apparently similar problems. This can be due to a variety of features. For instance, the ecological context of a problem will be interpreted differently by different species. This could relate to how they interpret the problem, but also, more basically, which cue they see as key. Differences in the latter may influence the ability to solve the task not because of variations in cognitive ability per se, but because one species has to first learn which cue is relevant before it is able to solve the task. In our previous work, cleaner fish learned faster than three species of primates to give an "ephemeral" food source priority over a "resident" food source, where the relevant cue was the plates (but the foods were identical). To determine the degree to which this cue influenced the primates' ability to learn the task, relative to cleaner fish, we here repeated the task with both capuchin monkeys and cleaners, using two variations designed to be more salient to capuchins (the cleaners were also tested to see if these changes negatively impacted their performance). In the first, we changed the cue from the plate presenting the food (original plate task) to the color of the food itself (now the plates were identical). In the second, we hid the food rewards, as primates are known to have difficulties inhibiting responses to visible rewards. Primates did improve their performance on both adapted tasks. Interestingly, and contrary to our predictions, fish performed at the same level across all versions of the task.

In comparative psychology, both similarities and differences among species are studied to better understand the evolution of their behavior. To do so, we first test species in tasks using similar procedures, but if differences are found, it is important to determine their underlying cause(s) (e.g., are they due to ecology, cognitive ability, an artifact of the study, and/or some other factor?). In our previous work, primates performed unexpectedly poorly on an apparently simple two-choice discrimination task based on the natural behavior of cleaner fish, while the fish did quite well. In this task, if the subjects first chose one of the options (ephemeral) they received both food items, but if they chose the other (permanent) option first, the ephemeral option disappeared. Here, we test several proposed explanations for primates' relatively poorer performance. In Study 1, we used a computerized paradigm that differed from the previous test by removing interaction with human experimenters, which may be distracting, and providing a more standardized testing environment. In Study 2, we adapted the computerized paradigm from Study 1 to be more relevant to primate ecology. Monkeys' overall performance in these adapted tasks matched the performance of the fish in the original study, showing that with the appropriate modifications they can solve the task. We discuss these results in light of comparative research, which requires balancing procedural similarity with considerations of how the details of the task or the context may influence how different species perceive and solve tasks differently.

The calcium-binding protein parvalbumin (PV) is a recognized marker of short-axon GABA-ergic neurons in the cortex and the hippocampus. However in addition, PV is expressed by excitatory, glutamatergic neurons in various areas of the brain and spinal cord. Depending on the location of these neurons, loading of their synaptic vesicles with glutamate is mediated by either of three vesicular glutamate transporters (VGlut): VGlut1, VGlut2, or VGlut3. Driven by our interest in one of these glutamatergic/PV-expressing cell clusters—the lateral hypothalamic parvafox nucleus—we investigated the functions of this population of neurons by the selective deletion of VGlut2 expression in PV-expressing cells according to the Cre/Lox-approach. PV-Cre;VGlut2-Lox mutant mice are phenotypically characterized by deficits in locomotion and vocalization, by a decreased thermal nociception, and by an increased social dominance. We conducted a search of the Allen Brain Atlas for regions that might co-express the genes encoding PV and VGlut2, and that might thus contribute to the manifestation of the observed phenotypes. Our survey revealed several structures that could contribute to the deficits in locomotion and vocalization, such as the red, the subthalamic and the deep cerebellar nuclei. It also disclosed that a shift in the balance of afferental glutamatergic neurotransmission to the periaqueductal gray matter might be accountable for the decrease in sensitivity to pain and for the increase in social dominance. As a whole, this study broadens the state of knowledge about PV-expressing excitatory neurons.