Evolution and function of neurocognitive systems in non-human animals.

The variety and richness of organisms found in nature offers scientists plenty of opportunities to investigate the many facets of biological complexity, and formulate novel research questions and hypotheses. This does not only apply to species-specific characteristics but, even more interestingly, to those features that can be observed across the animal kingdom. Comparative studies in psychology and neuroscience have proved to be an effective tool in advancing our understanding of the mechanisms underlying specific cognitive abilities, as well as their development, function, and evolution. This Collection gathers more than 40 contributions by scientists from all over the world, addressing different questions, in a variety of invertebrate and vertebrate species. The research comprises behavioural, electrophysiological, molecular, genetic, and neuroimaging studies, with the common aim of contributing to our understanding of the evolution and function of cognition.

Both the similarity and differences among species can help us understand the evolution of neurocognitive features and behaviours. Species as close to humans as primates enable scientists to look at brain structures and pathways (e.g., sulcal morphology[1]; fast visual responses in the amygdala[2]) and behavioural characteristics thought to be exclusive to our species (e.g., left-cradling bias[3]; lateral eye bias[4]; handedness[5]; abstract concept learning[6]), and investigate their neuroanatomical, genetic, and environmental basis (e.g., mutual gaze in social communication[7]). At the same time, the study and comparison of phylogenetically distant species, like birds or fish, can be ideal for testing predictions about the generality and conservation of brain mechanisms across the evolutionary tree (e.g., inhibition of return in barn owls[8]; Approximate Number System in zebrafish[9]; numerical discrimination in domestic chicks[10]; visual mental manipulation in Grey parrot, children, and human adults[11]). On the other hand, comparing related species may also reveal species-specific differences, that highlight the evolutionary divergence of neuronal circuit functions (e.g., the synaptic plasticity and the key molecules regulating it in shrews, mice, and bats[12]).

In some of the studies included in this Collection, the same tasks are presented to different species, revealing interesting inter-specific differences in the behavioural response (e.g., in re-orientation spatial skills in different species of fish[13]; in the use of geometric cues by rats and chicks[14]). Relatedly, comparative research of this sort sometimes raises questions about the conditions in which different species are tested. Some of the papers thus investigate potential methodological limitations in the study of animal behaviour. For instance, Morandi-Raikova and Mayer[15] show that experimental manipulation can affect the behaviour and the neural activity of the tested animal. It is also essential to provide replication of previous findings, either to substantiate the claims presented, or—as done by Lemaire[16] in this Collection—to question them.

Behavioural studies are extremely valuable in testing theories of adaptation (e.g., natural pedagogy in dogs[17]), emotional processing (e.g., in dogs[18]), rationality (e.g., in mice[19]), decision-making (e.g., in pigeons[20]), learning (e.g., in bees[21]), and memory (e.g., in cuttlefish[22]; in mice[23]), but they can also reveal intriguing possible relationships, such as between behaviour, brain mass, and lifespan, as shown by Kaplan[24] in Australian native birds. Animals raised in laboratories give scientists the possibility to study specific cognitive abilities in naïve individuals (e.g., the use of sensory cues in social learning in naïve gerbils[25]) and allow scientists to control for experience, especially in early life (e.g., the effect of early life stress on memory formation in the nematode C. elegans[26]; the effect of long-lasting social isolation and re-socialization on cognitive performance and brain activity in Octodon degus[27]). This is particularly valuable in precocial species such as chicken, which are ideal to investigate in-born predispositions to attend to specific stimuli (e.g.,[28]), and to exploit imprinting procedures to elucidate the ecological function of statistical learning (e.g.,[29]). Free living animals, on the other hand, allow scientists to study how species behave in their natural environment. Louder et al.[30] investigated behavioural plasticity and gene expression in response to different antagonistic stimuli in free-living red-winged blackbirds and found shared molecular and behavioural pathways involved in the recognition of—and reaction to—both evolutionarily old and new enemies. Wild-caught and laboratory individuals of the same species can also be tested to compare the possible group-specific performances in cognitive tasks, as shown in the study by Rössler and colleagues[31], who investigated the ability to innovate in Goffin’s cockatoos. Furthermore, through the study of groups of animals of the same species living in different habitats, it is possible to assess the effect of the environment on behaviour (e.g., the behavioural adjustment of striped field mice to human disturbance[32]).

Notably, behavioural studies can be combined with molecular, electrophysiological, neuro-imaging, and genetic techniques to pinpoint the neural mechanisms underpinning behaviour (e.g., immediate early gene expression of multi-component behaviour in pigeons[33]; protein products of the immediate early genes in response to exposure to conspecific contact calls in male budgerigars[34]; electrophysiological recordings of neuronal activity during song broadcast and social relationships in starlings[35]; cortical activity and motor behaviour to establish levels of arousal in rodents[36]). Furthermore, they can be used to investigate the effects of a treatment on behaviour (e.g., chronic consumption of D-amino acids on spatial learning and expression of NMDA receptors in mice[37]) and on their neural signature (e.g., anxiolytic high-frequency electrical stimulation of the bed nucleus of the stria terminalis in rats on c-Fos expression[38]). Some species can be manipulated so that they express a marker such as GFP, in specific subpopulations of neurons, in order to study their differentiation and development (e.g., sex-differences in hippocampal neurons in mice[39]); whereas in other species, genetic lines in which a particular gene is silenced can be produced, which is invaluable for providing insights into the genetic substrates of specific neurobiological features or behaviours (e.g., lateralization in Drosophila[40]; impulsivity in rats[41]).

The papers published in this Collection highlight how fundamental studies on animal models are to our understanding of the functioning, development, and evolution of neurocognitive systems, and teach us, through the comparative approach, that we share more than we think with even the more evolutionarily distant species.