Serial reversal learning in nectar-feeding bats.

We explored the behavioral flexibility of Commissaris's long-tongued bats through a spatial serial reversal foraging task. Bats kept in captivity for short periods were trained to obtain nectar rewards from two artificial flowers. At any given time, only one of the flowers provided rewards and these reward contingencies reversed in successive blocks of 50 flower visits. All bats detected and responded to reversals by making most of their visits to the currently active flower. As the bats experienced repeated reversals, their preference re-adjusted faster. Although the flower state reversals were theoretically predictable, we did not detect anticipatory behavior, that is, frequency of visits to the alternative flower did not increase within each block as the programmed reversal approached. The net balance of these changes was a progressive improvement in performance in terms of the total proportion of visits allocated to the active flower. The results are compatible with, but do not depend on, the bats displaying an ability to 'learn to learn' and show that the dynamics of allocation of effort between food sources can change flexibly according to circumstances.

Object play and problem solving in infancy: Insights into tool use.

Tool use is primarily, but not exclusively, present in species with otherwise advanced cognitive traits. However, the interaction between such traits and conspecific inter-individual variation in the presence, complexity, or intensity of tool use is far from being established. We addressed this matter among human infants, seeking factors that relate to differences in tool use. We examined, both correlationally and experimentally, whether the propensity to engage in object combinations predicts performance in means-end problem-solving tasks involving or not involving the use of a tool. We tested 71 infants aged 15, 18, 21, and 24 months, dividing them into two subgroups: one exposed to an adult demonstrating object-object combinations (i.e., "prompting" infants to combine objects together) and another with comparable social exposure but where the adult demonstrated single-object manipulations. We found a correlation between the combined level of spontaneous and prompted object combinations and problem-solving performance regardless of the involvement of tools in the problem. However, we did not find differences in tool-use performance between the two demonstration subgroups. The correlational analysis suggests that complexity of play, as measured by the frequency of combining objects, is linked to infants' problem-solving skills rather than being specifically associated with tool use, as previously suggested in the literature.

GoFish: A low-cost, open-source platform for closed-loop behavioural experiments on fish.

Fish are the most species-rich vertebrate group, displaying vast ecological, anatomical and behavioural diversity, and therefore are of major interest for the study of behaviour and its evolution. However, with respect to other vertebrates, fish are relatively underrepresented in psychological and cognitive research. A greater availability of easily accessible, flexible, open-source experimental platforms that facilitate the automation of task control and data acquisition may help to reduce this bias and improve the scalability and refinement of behavioural experiments in a range of different fish species. Here we present GoFish, a fully automated platform for behavioural experiments in aquatic species. GoFish includes real-time video tracking of subjects, presentation of stimuli in a computer screen, an automatic feeder device, and closed-loop control of task contingencies and data acquisition. The design and software components of the platform are freely available, while the hardware is open-source and relatively inexpensive. The control software, Bonsai, is designed to facilitate rapid development of task workflows and is supported by a growing community of users. As an illustration and test of its use, we present the results of two experiments on discrimination learning, reversal, and choice in goldfish (Carassius auratus). GoFish facilitates the automation of high-throughput protocols and the acquisition of rich behavioural data. Our platform has the potential to become a widely used tool that facilitates complex behavioural experiments in aquatic species.

Choosing fast and simply: Construction of preferences by starlings through parallel option valuation.

The integration of normative and descriptive analyses of decision processes in humans struggles with the fact that measuring preferences by different procedures yields different rankings and that humans appear irrationally impulsive (namely, show maladaptive preference for immediacy). Failure of procedure invariance has led to the widespread hypothesis that preferences are constructed "on the spot" by cognitive evaluations performed at choice time, implying that choices should take extra time in order to perform the necessary comparisons. We examine this issue in experiments with starlings (Sturnus vulgaris) and show that integrating normative and descriptive arguments is possible and may help reinterpreting human decision results. Our main findings are that (1) ranking alternatives through direct rating (response time) accurately predicts preference in choice, overcoming failures of procedure invariance; (2) preference is not constructed at choice time nor does it involve extra time (we show that the opposite is true); and (3) starlings' choices are not irrationally impulsive but are instead directly interpretable in terms of profitability ranking. Like all nonhuman research, our protocols examine decisions by experience rather than by description, and hence support the conjecture that irrationalities that prevail in research with humans may not be observed in decisions by experience protocols.

Testing cognitive models of decision-making: selected studies with starlings.

The behavioural sciences are home to controversies that have survived for centuries, notably about the relation between observable behaviour and theoretical constructs addressing out-of-sight processes in the agents' brains. There is no shared definition for cognition, but the very existence of a thriving journal called Animal Cognition proves that such controversies are still live and help to (a) promote research on the complexity of processes leading to action, and (b) nudge scholars to restrict their cognitive models to those that can be falsified experimentally. Here, we illustrate some of these issues in a limited arena, focusing on the construction and expression of subjective value and choice. Using mainly work from our own laboratory, we show that valuation of alternatives is sensitive to options' properties, to subject's state, and to background alternatives. These factors exert their influence at the time the subject learns about individual options, rather than at choice time. We also show that valuation can be experimentally dissociated from the cognitive representation of options' metrics and argue that experimental animals process options independently at the time of choice, without elaborated comparisons along different dimensions. The findings we report are not consistent with the hypothesis that preference is constructed at the time of choice, a prevalent view in human decision-making research. We argue that animal cognition, viewed as a research program at the crossroads of different behavioural sciences rather than as a debate about properties of mental life, is inspiring and solid, and a progressive and progressing paradigm.

Paradoxical choice and the reinforcing value of information.

Signals that reduce uncertainty can be valuable because well-informed decision-makers can better align their preferences to opportunities. However, some birds and mammals display an appetite for informative signals that cannot be used to increase returns. We explore the role that reward-predictive stimuli have in fostering such preferences, aiming at distinguishing between two putative underlying mechanisms. The 'information hypothesis' proposes that reducing uncertainty is reinforcing per se, somewhat consistently with the concept of curiosity: a motivation to know in the absence of tractable extrinsic benefits. In contrast, the 'conditioned reinforcement hypothesis', an associative account, proposes asymmetries in secondarily acquired reinforcement: post-choice stimuli announcing forthcoming rewards (S+) reinforce responses more than stimuli signalling no rewards (S-) inhibit responses. In three treatments, rats faced two equally profitable options delivering food probabilistically after a fixed delay. In the informative option (Info), food or no food was signalled immediately after choice, whereas in the non-informative option (NoInfo) outcomes were uncertain until the delay lapsed. Subjects preferred Info when (1) both outcomes were explicitly signalled by salient auditory cues, (2) only forthcoming food delivery was explicitly signalled, and (3) only the absence of forthcoming reward was explicitly signalled. Acquisition was slower in (3), when food was not explicitly signalled, showing that signals for positive outcomes have a greater influence on the development of preference than signals for negative ones. Our results are consistent with an elaborated conditioned reinforcement account, and with the conjecture that both uncertainty reduction and conditioned reinforcement jointly act to generate preference.

Sex differences in the use of spatial cues in two avian brood parasites.

Shiny and screaming cowbirds are avian interspecific brood parasites that locate and prospect host nests in daylight and return from one to several days later to lay an egg during the pre-dawn twilight. Thus, during nest location and prospecting, both location information and visual features are available, but the latter become less salient in the low-light conditions when the nests are visited for laying. This raises the question of how these different sources of information interact, and whether this reflects different behavioural specializations across sexes. Differences are expected, because in shiny cowbirds, females act alone, but in screaming cowbirds, both sexes make exploratory and laying nest visits together. We trained females and males of shiny and screaming cowbird to locate a food source signalled by both colour and position (cues associated), and evaluated performance after displacing the colour cue to make it misleading (cues dissociated). There were no sex or species differences in acquisition performance while the cues were associated. When the colour cue was relocated, individuals of both sexes and species located the food source making fewer visits to non-baited wells than expected by chance, indicating that they all retained the position as an informative cue. In this phase, however, shiny cowbird females, but not screaming, outperformed conspecific males, visiting fewer non-baited wells before finding the food location and making straighter paths in the search. These results are consistent with a greater reliance on spatial memory, as expected from the shiny cowbird female's specialization on nest location behaviour.

Imprinting on time-structured acoustic stimuli in ducklings.

Filial imprinting is a dedicated learning process that lacks explicit reinforcement. The phenomenon itself is narrowly heritably canalized, but its content, the representation of the parental object, reflects the circumstances of the newborn. Imprinting has recently been shown to be even more subtle and complex than previously envisaged, since ducklings and chicks are now known to select and represent for later generalization abstract conceptual properties of the objects they perceive as neonates, including movement pattern, heterogeneity and inter-component relationships of same or different. Here, we investigate day-old Mallard (Anas platyrhynchos) ducklings' bias towards imprinting on acoustic stimuli made from mallards' vocalizations as opposed to white noise, whether they imprint on the temporal structure of brief acoustic stimuli of either kind, and whether they generalize timing information across the two sounds. Our data are consistent with a strong innate preference for natural sounds, but do not reliably establish sensitivity to temporal relations. This fits with the view that imprinting includes the establishment of representations of both primary percepts and selective abstract properties of their early perceptual input, meshing together genetically transmitted prior pre-dispositions with active selection and processing of the perceptual input.

Ducklings imprint on chromatic heterogeneity.

Avian filial imprinting is a rapid form of learning occurring just after hatching in precocial bird species. The acquired imprint on either or both parents goes on to affect the young bird's survival and social behaviour later in life (Bateson in Biol Rev 41:177-217, 1966). The imprinting mechanism is specialized but flexible, and causes the hatchling to develop high-fidelity recognition and attraction to any moving stimulus of suitable size seen during a predefined sensitive period. It has been observed (Martinho and Kacelnik in Science 353:286-288, 2016; Versace et al. in Anim Cogn 20:521-529, 2017) that in addition to visual and acoustic sensory inputs, imprinting may incorporate informational rules or abstract concepts. Here we report a study of mallard ducklings (Anas platyrhynchos domesticus) undergoing imprinting on the chromatic heterogeneity of stimuli, with a focus on how this may be transferred to novel objects. Ducklings were exposed to a series of chromatically heterogeneous or homogeneous stimuli and tested for preference between two novel stimuli, one heterogeneous and the other homogeneous. Exposure to heterogeneity significantly enhanced preference for novel heterogeneous stimuli, relative to ducklings exposed to homogeneous stimuli or unexposed controls. These findings support the view that imprinting does not rely solely on exemplars, or snapshot-like representations of visual input, but that instead young precocial animals form complex multidimensional representations of the target object, involving abstract properties, either at the time of learning, or later, through generalization from the learnt exemplars.

Goffin's cockatoos make the same tool type from different materials.

Innovative tool manufacture is rare and hard to isolate in animals. We show that an Indonesian generalist parrot, the Goffin's cockatoo, can flexibly and spontaneously transfer the manufacture of stick-type tools across three different materials. Each material required different manipulation patterns, including substrates that required active sculpting for achieving a functional, elongated shape.

Asymmetric visual input and route recapitulation in homing pigeons.

Pigeons (Columba livia) display reliable homing behaviour, but their homing routes from familiar release points are individually idiosyncratic and tightly recapitulated, suggesting that learning plays a role in route establishment. In light of the fact that routes are learned, and that both ascending and descending visual pathways share visual inputs from each eye asymmetrically to the brain hemispheres, we investigated how information from each eye contributes to route establishment, and how information input is shared between left and right neural systems. Using on-board global positioning system loggers, we tested 12 pigeons' route fidelity when switching from learning a route with one eye to homing with the other, and back, in an A-B-A design. Two groups of birds, trained first with the left or first with the right eye, formed new idiosyncratic routes after switching eyes, but those that flew first with the left eye formed these routes nearer to their original routes. This confirms that vision plays a major role in homing from familiar sites and exposes a behavioural consequence of neuroanatomical asymmetry whose ontogeny is better understood than its functional significance.

Visual attention and the acquisition of information in human crowds.

Pedestrian crowds can form the substrate of important socially contagious behaviors, including propagation of visual attention, violence, opinions, and emotional state. However, relating individual to collective behavior is often difficult, and quantitative studies have largely used laboratory experimentation. We present two studies in which we tracked the motion and head direction of 3,325 pedestrians in natural crowds to quantify the extent, influence, and context dependence of socially transmitted visual attention. In our first study, we instructed stimulus groups of confederates within a crowd to gaze up to a single point atop of a building. Analysis of passersby shows that visual attention spreads unevenly in space and that the probability of pedestrians adopting this behavior increases as a function of stimulus group size before saturating for larger groups. We develop a model that predicts that this gaze response will lead to the transfer of visual attention between crowd members, but it is not sufficiently strong to produce a tipping point or critical mass of gaze-following that has previously been predicted for crowd dynamics. A second experiment, in which passersby were presented with two stimulus confederates performing suspicious/irregular activity, supports the predictions of our model. This experiment reveals that visual interactions between pedestrians occur primarily within a 2-m range and that gaze-copying, although relatively weak, can facilitate response to relevant stimuli. Although the above aspects of gaze-following response are reproduced robustly between experimental setups, the overall tendency to respond to a stimulus is dependent on spatial features, social context, and sex of the passerby.

Starlings uphold principles of economic rationality for delay and probability of reward.

Rationality principles are the bedrock of normative theories of decision-making in biology and microeconomics, but whereas in microeconomics, consistent choice underlies the notion of utility; in biology, the assumption of consistent selective pressures justifies modelling decision mechanisms as if they were designed to maximize fitness. In either case, violations of consistency contradict expectations and attract theoretical interest. Reported violations of rationality in non-humans include intransitivity (i.e. circular preferences) and lack of independence of irrelevant alternatives (changes in relative preference between options when embedded in different choice sets), but the extent to which these observations truly represent breaches of rationality is debatable. We tested both principles with starlings (Sturnus vulgaris), training subjects either with five options differing in food delay (exp. 1) or with six options differing in reward probability (exp. 2), before letting them choose repeatedly one option out of several binary and trinary sets of options. The starlings conformed to economic rationality on both tests, showing strong stochastic transitivity and no violation of the independence principle. These results endorse the rational choice and optimality approaches used in behavioural ecology, and highlight the need for functional and mechanistic enquiring when apparent violations of such principles are observed.

Context-dependent utility overrides absolute memory as a determinant of choice.

A core problem of decision theories is that although decisionmakers' preferences depend on learning, their choices could be driven either by learned representations of the physical properties of each alternative (for instance reward sizes) or of the benefit (utility and fitness) experienced from them. Physical properties are independent of the subject's state and context, but utility depends on both. We show that starlings' choices are better explained by memory for context-dependent utility than by representations of the alternatives' physical properties, even when the decisionmakers' state is controlled and they have accurate knowledge about the options' physical properties. Our results support the potential universality of utility-driven preference control.

Navigating in a volumetric world: metric encoding in the vertical axis of space.

Animals navigate through three-dimensional environments, but we argue that the way they encode three-dimensional spatial information is shaped by how they use the vertical component of space. We agree with Jeffery et al. that the representation of three-dimensional space in vertebrates is probably bicoded (with separation of the plane of locomotion and its orthogonal axis), but we believe that their suggestion that the vertical axis is stored "contextually" (that is, not containing distance or direction metrics usable for novel computations) is unlikely, and as yet unsupported. We describe potential experimental protocols that could clarify these differences in opinion empirically.

Brood parasite eggs enhance egg survivorship in a multiply parasitized host.

Despite the costs to avian parents of rearing brood parasitic offspring, many species do not reject foreign eggs from their nests. We show that where multiple parasitism occurs, rejection itself can be costly, by increasing the risk of host egg loss during subsequent parasite attacks. Chalk-browed mockingbirds (Mimus saturninus) are heavily parasitized by shiny cowbirds (Molothrus bonariensis), which also puncture eggs in host nests. Mockingbirds struggle to prevent cowbirds puncturing and laying, but seldom remove cowbird eggs once laid. We filmed cowbird visits to nests with manipulated clutch compositions and found that mockingbird eggs were more likely to escape puncture the more cowbird eggs accompanied them in the clutch. A Monte Carlo simulation of this 'dilution effect', comparing virtual hosts that systematically either reject or accept parasite eggs, shows that acceptors enjoy higher egg survivorship than rejecters in host populations where multiple parasitism occurs. For mockingbirds or other hosts in which host nestlings fare well in parasitized broods, this benefit might be sufficient to offset the fitness cost of rearing parasite chicks, making egg acceptance evolutionarily stable. Thus, counterintuitively, high intensities of parasitism might decrease or even reverse selection pressure for host defence via egg rejection.

Pro-sociality without empathy.

Empathy, the capacity to recognize and share feelings experienced by another individual, is an important trait in humans, but is not the same as pro-sociality, the tendency to behave so as to benefit another individual. Given the importance of understanding empathy's evolutionary emergence, it is unsurprising that many studies attempt to find evidence for it in other species. To address the question of what should constitute evidence for empathy, we offer a critical comparison of two recent studies of rescuing behaviour that report similar phenomena but are interpreted very differently by their authors. In one of the studies, rescue behaviour in rats was interpreted as providing evidence for empathy, whereas in the other, rescue behaviour in ants was interpreted without reference to sharing of emotions. Evidence for empathy requires showing that actor individuals possess a representation of the receiver's emotional state and are driven by the psychological goal of improving its wellbeing. Proving psychological goal-directedness by current standards involves goal-devaluation and causal sensitivity protocols, which, in our view, have not been implemented in available publications. Empathy has profound significance not only for cognitive and behavioural sciences but also for philosophy and ethics and, in our view, remains unproven outside humans.

New Caledonian crows use tools for non-foraging activities.

Tool use is of great interest for cognitive research, largely because it can be particularly revealing about the underlying information processing mechanisms. Tool use that is inflexible or requires extensive experience to change, and that is only addressed towards specific targets such as food, is not likely to reflect unusual or particularly complex cognition. On the contrary, if tools are employed flexibly and for a variety of innovative purposes, then conventional combinations of inherited predispositions and associative learning are challenged and interesting questions emerge. Since New Caledonian crows (Corvus moneduloides) are especially adept at using and making tools for food extraction, we decided to examine their ability to generalise this to other contexts. We recorded how five pairs of New Caledonian crows interacted with novel objects that were not associated with food. We observed eight occasions in which the first contact with the novel object was mediated by a tool, suggesting that the function of the tool was for exploration. This is the first report of non-foraging tool use in New Caledonian crows, and it implies that the cognitive operations controlling tool-oriented behaviour in this species are more general than previously thought.

Behavioural ecology: tool manufacture by naive juvenile crows.

New Caledonian crows (Corvus moneduloides) are the most prolific avian tool-users. Regional variation in the shape of their tools may be the result of cumulative cultural evolution--a phenomenon considered to be a hallmark of human culture. Here we show that hand-raised juvenile New Caledonian crows spontaneously manufacture and use tools, without any contact with adults of their species or any prior demonstration by humans. Our finding is a crucial step towards producing informed models of cultural transmission in this species, and in animals in general.

Sex differences in learning flexibility in an avian brood parasite, the shiny cowbird.

Females of brood parasitic shiny cowbirds, Molothrus bonariensis, search and prospect host nests, synchronizing parasitism with host laying. This behavior is sex-specific, as females perform this task without male's assistance. Host nests must be removed from the female's memory "library" after being parasitized, to avoid repeated parasitism, or when they become unavailable because of predation. Thus, females must adjust their stored information about host nest status more dynamically than males, possibly leading to differences in learning flexibility. We tested for sex differences in a visual (local cues) and a spatial discrimination reversal learning task, expecting females to outperform males as an expression of greater behavioral flexibility. Both sexes learned faster the spatial than the visual task during both acquisition and reversal. In the visual task there were no sex differences in acquisition, but females reversed faster than males. In the spatial task there were no sex differences during either acquisition or reversal, possibly because of a ceiling effect: both sexes learned too fast for differences in performance to be detectable. Faster female reversal in a visual but not spatial task indicates that the greater behavioral flexibility in females may only be detectable above some level of task difficulty.