Life is in motion (through a chick's eye).

Cognitive scientists, social psychologists, computer scientists, neuroscientists, ethologists and many others have all wondered how brains detect and interpret the motion of living organisms. It appears that specific cues, incorporated into our brains by natural selection, serve to signal the presence of living organisms. A simple geometric figure such as a triangle put in motion with specific kinematic rules can look alive, and it can even seem to have intentions and goals. In this article, we survey decades of parallel investigations on the motion cues that drive animacy perception-the sensation that something is alive-in non-human animals, especially in precocial species, such as the domestic chick, to identify inborn biological predispositions. At the same time, we highlight the relevance of these studies for an understanding of human typical and atypical cognitive development.

Spontaneous preference for unpredictability in the temporal contingencies between agents' motion in naive domestic chicks.

The ability to recognize animate agents based on their motion has been investigated in humans and animals alike. When the movements of multiple objects are interdependent, humans perceive the presence of social interactions and goal-directed behaviours. Here, we investigated how visually naive domestic chicks respond to agents whose motion was reciprocally contingent in space and time (i.e. the time and direction of motion of one object can be predicted from the time and direction of motion of another object). We presented a 'social aggregation' stimulus, in which three smaller discs repeatedly converged towards a bigger disc, moving in a manner resembling a mother hen and chicks (versus a control stimulus lacking such interactions). Remarkably, chicks preferred stimuli in which the timing of the motion of one object could not be predicted by that of other objects. This is the first demonstration of a sensitivity to the temporal relationships between the motion of different objects in naive animals, a trait that could be at the basis of the development of the perception of social interaction and goal-directed behaviours.

Visual Field Analysis: A reliable method to score left and right eye use using automated tracking.

Brain and behavioural asymmetries have been documented in various taxa. Many of these asymmetries involve preferential left and right eye use. However, measuring eye use through manual frame-by-frame analyses from video recordings is laborious and may lead to biases. Recent progress in technology has allowed the development of accurate tracking techniques for measuring animal behaviour. Amongst these techniques, DeepLabCut, a Python-based tracking toolbox using transfer learning with deep neural networks, offers the possibility to track different body parts with unprecedented accuracy. Exploiting the potentialities of DeepLabCut, we developed Visual Field Analysis, an additional open-source application for extracting eye use data. To our knowledge, this is the first application that can automatically quantify left-right preferences in eye use. Here we test the performance of our application in measuring preferential eye use in young domestic chicks. The comparison with manual scoring methods revealed a near perfect correlation in the measures of eye use obtained by Visual Field Analysis. With our application, eye use can be analysed reliably, objectively and at a fine scale in different experimental paradigms.

Steps towards a computational ethology: an automatized, interactive setup to investigate filial imprinting and biological predispositions.

Soon after hatching, the young of precocial species, such as domestic chicks or ducklings, learn to recognize their social partner by simply being exposed to it (imprinting process). Even artificial objects or stimuli displayed on monitor screens can effectively trigger filial imprinting, though learning is canalized by spontaneous preferences for animacy signals, such as certain kinds of motion or a face-like appearance. Imprinting is used as a behavioural paradigm for studies on memory formation, early learning and predispositions, as well as number and space cognition, and brain asymmetries. Here, we present an automatized setup to expose and/or test animals for a variety of imprinting experiments. The setup consists of a cage with two high-frequency screens at the opposite ends where stimuli are shown. Provided with a camera covering the whole space of the cage, the behaviour of the animal is recorded continuously. A graphic user interface implemented in Matlab allows a custom configuration of the experimental protocol, that together with Psychtoolbox drives the presentation of images on the screens, with accurate time scheduling and a highly precise framerate. The setup can be implemented into a complete workflow to analyse behaviour in a fully automatized way by combining Matlab (and Psychtoolbox) to control the monitor screens and stimuli, DeepLabCut to track animals' behaviour, Python (and R) to extract data and perform statistical analyses. The automated setup allows neuro-behavioural scientists to perform standardized protocols during their experiments, with faster data collection and analyses, and reproducible results.

Response of male and female domestic chicks to change in the number (quantity) of imprinting objects.

When facing two sets of imprinting objects of different numerousness, domestic chicks prefer to approach the larger one. Given that choice for familiar and novel stimuli in imprinting situations is known to be affected by the sex of the animals, we investigated how male and female domestic chicks divide the time spent in the proximity of a familiar versus an unfamiliar number of objects, and how animals interact (by pecking) with these objects. We confirmed that chicks discriminate among the different numerousnesses, but we also showed that females and males behave differently, depending on the degree of familiarity of the objects. When objects in the testing sets were all familiar, females equally explored both sets and pecked at all objects individually. Males instead selectively approached the familiar numerousness and pecked more at it. When both testing sets comprised familiar as well as novel objects, both males and females approached the larger numerousness of familiar objects. However, chicks directed all their pecks toward the novel object within the set. Differences in the behavior of males and females can be accounted for in terms of sex difference in the motivation to reinstate social contact with the familiar objects and to explore novel ones, likely associated with the ecology and the social structure of the species before domestication.

Innate sensitivity to face-to-face biological motion.

Sensitivity to face-to-face stimuli configurations, which likely indicates interaction, seems to appear early in infants' development, and recently a preference for face-to-face (vs. other spatial configurations) has been shown to occur in macaque monkeys. It is unknown, however, whether such a preference is acquired through experience or as an evolutionary-given biological predisposition. Here, we exploited a precocial social animal, the domestic chick, as a model system to address this question. Visually naive chicks were tested for their spontaneous preferences for face-to-face vs. back-to-back hen dyads of point-light displays depicting biological motion. We found that female chicks have a spontaneous preference for the facing interactive configuration. Males showed no preference, as expected due to the well-known low social motivation of males in this highly polygynous species. These findings support the idea of an innate and sex-dependent predisposition toward social and interacting stimuli in a vertebrate brain such as that of chicks.

Stability and individual variability of social attachment in imprinting.

Filial imprinting has become a model for understanding memory, learning and social behaviour in neonate animals. This mechanism allows the youngs of precocial bird species to learn the characteristics of conspicuous visual stimuli and display affiliative response to them. Although longer exposures to an object produce stronger preferences for it afterwards, this relation is not linear. Sometimes, chicks even prefer to approach novel rather than familiar objects. To date, little is known about how filial preferences develop across time. This study aimed to investigate filial preferences for familiar and novel imprinting objects over time. After hatching, chicks were individually placed in an arena where stimuli were displayed on two opposite screens. Using an automated setup, the duration of exposure and the type of stimuli were manipulated while the time spent at the imprinting stimulus was monitored across 6 days. We showed that prolonged exposure (3 days vs 1 day) to a stimulus produced robust filial imprinting preferences. Interestingly, with a shorter exposure (1 day), animals re-evaluated their filial preferences in functions of their spontaneous preferences and past experiences. Our study suggests that predispositions influence learning when the imprinting memories are not fully consolidated, driving animal preferences toward more predisposed stimuli.

Sensitive periods for social development: Interactions between predisposed and learned mechanisms.

We analysed research that makes use of precocial species as animal models to describe the interaction of predisposed mechanisms and environmental factors in early learning, in particular for the development of social cognition. We also highlight the role of sensitive periods in this interaction, focusing on domestic chicks as one of the main animal models for this field. In the first section of the review, we focus on the emergence of early predispositions to attend to social partners. These attentional biases appear before any learning experience about social stimuli. However, non-specific experiences occurring during sensitive periods of the early post-natal life determine the emergence of these predisposed mechanisms for the detection of social partners. Social predispositions have an important role for the development learning-based social cognitive functions, showing the interdependence of predisposed and learned mechanisms in shaping social development. In the second part of the review we concentrate on the reciprocal interactions between filial imprinting and spontaneous (not learned) social predispositions. Reciprocal influences between these two sets of mechanisms ensure that, in the natural environment, filial imprinting will target appropriate social objects. Neural and physiological mechanisms regulating the sensitive periods for the emergence of social predispositions and for filial imprinting learning are also described.

No evidence of spontaneous preference for slowly moving objects in visually naïve chicks.

It has been recently reported that young chicks that have received equal exposure to slowly- and fast-rotating objects showed a preference for slowly-rotating objects. This would suggest that visual experience with slowly moving objects is necessary for object recognition in newborns. I attempted to duplicate this finding in newborn chicks using a simple rotating blue cube. No significant preference was found. Using objects similar to the ones used in the previous study (digital embryos), I observed a strong and robust preference for the fast- (not for the slow-) rotating object. To clarify whether the discrepancies with the previous study could be due to the stimuli frame-frequency used (the chicks' visual system is characterized by high temporal resolution), I repeated the experiments by presenting the stimuli with a lower-frame frequency (from 120 fps to 24 fps). However, similar preferences for the fast-rotating objects were found, this time also for the rotating blue cube. These results suggest a preference for fast-rotating objects that is modulated by the shape and, in part, by the frame-frequency. It remains to be established whether the discrepancies between this study and the previous study can be explained by differences related to strains or artefacts due to the use of monitors with a low-refresh rate.

Statistical learning in domestic chicks is modulated by strain and sex.

Statistical learning is a key mechanism for detecting regularities from a variety of sensory inputs. Precocial newborn domestic chicks provide an excellent model for (1) exploring unsupervised forms of statistical learning in a comparative perspective, and (2) elucidating the ecological function of statistical learning using imprinting procedures. Here we investigated the role of the sex of the chicks in modulating the direction of preference (for familiarity or novelty) in a visual statistical learning task already employed with chicks and human infants. Using both automated tracking and direct human coding, we confirmed chicks' capacity to recognize the presence of a statistically defined structure underlying a continuous stream of shapes. Using a different chicken strain than previous studies, we were also able to highlight sex differences in chicks' propensity to approach the familiar or novel sequence. This could also explain a previous failure to reveal statistical learning in chicks which sex was however not determined. Our study confirms chicks' ability to track visual statistics. The pivotal role of sex in determining familiarity or novelty preferences in this species and the interaction with the animals' strain highlight the importance to contextualize comparative research within the ecology of each species.