Orsola Rosa-Salva

Lateralization of social cognition in the domestic chicken (Gallus gallus)

In this paper, we report on the ongoing work in our laboratories on the effect of lateralization produced by light exposure in the egg on social cognition in the domestic chick (Gallus gallus). The domestic chick possesses a lateralized visual system. This has effects on the chicks perception towards and interaction with its environment. This includes its ability to live successfully within a social group. We show that there is a tendency for right brain hemisphere dominance when performing social cognitive actions. As such, chicks show a left hemispatial bias for approaching a signalled target object, tend to perceive gaze and faces of human-like masks more effectively when using their left eye, are able to inhibit a pecking response more effectively when viewing a neighbour tasting a bitter substance with their left eye, and are better able to perform a transitive inference task when exposed to light in the egg and when forced to use their left eye only compared to dark-hatched or right eye chicks. Some of these effects were sex specific, with male chicks tending to show an increased effect of lateralization on their behaviours. These data are discussed in terms of overall social cognition in group living.

Filial responses as predisposed and learned preferences: Early attachment in chicks and babies

HighlightsPredispositions orient newborn babies and chicks towards animate objects.Subcortical/subpallial structures may be sufficient to support social predispositions.Social Behaviour Network areas might be involved in unlearnt social behaviours.Hormones facilitate preferences for predisposed stimuli and social attachment.Social predispositions are impaired in newborns at high genetic risk for autism. Abstract To what extent are filial responses the outcome of spontaneous or acquired preferences? The case of domestic chicks illustrates the connection between predisposed and learned knowledge in early social responses. In the absence of specific experience, chicks prefer to approach objects that are more similar to natural social partners (e.g. they prefer face‐like configurations, biological motion, self‐propelled objects and those that move at variable speed). Spontaneous preferences are complemented by filial imprinting, a powerful learning mechanism that enables chicks to quickly learn the features of specific social partners. While neurobiological studies have clarified that the substrates of spontaneous and learned preferences are at least partially distinct in chicks, evidence shows that spontaneous preferences might orient and facilitate imprinting on animate stimuli, such as the mother hen, and that hormones facilitate and strengthen preferences for predisposed stimuli. Preferences towards animate stimuli are observed in human neonates as well. The remarkable consistency between the perceptual cues attended to by newborn babies and naïve chicks suggests that the attentional biases observed in babies are unlikely to result from very rapid post‐natal learning, and confirms that research on precocial species can inform and guide human infant research with regards to both typical and atypical development. This has potentially important biomedical implications, opening new possibilities for the early detection of subjects at risk for autism spectrum disorders. We show how the parallel investigation of predispositions in naïve chicks and human infants, both benefiting from contact with social partners since the beginning of life, has greatly improved our understanding of early responses to social stimuli at the behavioural and neurobiological level.

Generalization of visual regularities in newly hatched chicks (Gallus gallus)

Evidence of learning and generalization of visual regularities in a newborn organism is provided in the present research. Domestic chicks have been trained to discriminate visual triplets of simultaneously presented shapes, implementing AAB versus ABA (Experiment 1), AAB versus ABB and AAB versus BAA (Experiment 2). Chicks distinguished pattern-following and pattern-violating novel test triplets in all comparisons, showing no preference for repetition-based patterns. The animals generalized to novel instances even when the patterns compared were not discriminable by the presence or absence of reduplicated elements or by symmetry (e.g., AAB vs. ABB). These findings represent the first evidence of learning and generalization of regularities at the onset of life in an animal model, revealing intriguing differences with respect to human newborns and infants. Extensive prior experience seems to be unnecessary to drive the process, suggesting that chicks are predisposed to detect patterns characterizing the visual world.

Dynamic features of animate motion activate septal and preoptic areas in visually naïve chicks (Gallus gallus)

The septum is an evolutionarily well-conserved part of the limbic system. It is known to be involved in many aspects of social behavior and is considered a key node of the social behavior network, together with the preoptic area. Involvement of these two brain regions has been recently observed in newly hatched chicks exposed to the natural motion of a living conspecific. However, it is unknown whether these areas respond also to simple motion cues that elicit animacy perception in humans and social predispositions in chicks. For example, naïve chicks are attracted by visual objects that appear to spontaneously change their speed (an index of self-propulsion, typical of animate creatures). Here we show that the right septum and the preoptic area of newly hatched visually naïve chicks exposed to speed changes have higher neuronal activity (revealed by c-Fos expression), compared with that of chicks exposed to constant motion. We thus found an involvement of these two areas in the perception of motion cues associated with animacy in newly hatched chicks without any previous visual experience. This demonstrates their early involvement in processing simple motion cues that allow the detection of animate creatures and elicit social predispositions in this animal model, as well as preferential attention in human infants and the perception of animacy in human adults.

The motion of a living conspecific activates septal and preoptic areas in naive domestic chicks (Gallus gallus)

Predispositions to attend to animate objects are ubiquitous in newborn vertebrates, but little is known about their neural bases. In this study, we wanted to know if exposure to the motion of a living, behaving conspecific will selectively activate septal, preoptic and amygdaloid areas in visually naive domestic chicks. For this purpose, newly hatched chicks were exposed to a live conspecific, whose natural motion presents of course several features typical of animate motion to which chicks are known to be sensitive. In the control group, chicks were exposed to a rotating stuffed chick that showed rigid non‐biological motion. The two stimuli were visually matched with regard to their static features. We measured brain activity by visualizing the immediate early gene product c‐Fos with a standard immunohistochemical procedure. Notably, dorsal right septum and left preoptic area showed higher activation in experimental subjects compared to the control animals. This is, to the best of our knowledge, the first demonstration of septal and preoptic areas involvement in response to the animate motion of a social partner, as opposed to rigid motion of a similarly looking stimulus. Moreover, these results indicate that previous visual experience and specific learning events are not necessary to establish the septal and preoptic areas function, which is present shortly after birth.

First exposure to an alive conspecific activates septal and amygdaloid nuclei in visually-naïve domestic chicks (Gallus gallus).

HighlightsSeptal and amygdaloid nuclei are involved in social behavior of adult animals.Here we investigated their involvement in early social responses of visually naive chicks.Higher activity in septum and amygdaloid nuclei of chicks after the first brief exposure to an alive conspecific. ABSTRACT The septal nuclei are an evolutionarily well‐conserved part of the limbic system, present in all vertebrate groups. Functionally, septal nuclei are involved in many important aspects of social behavior and lateral septum is considered a node of the social decision making network, together with amygdaloid nuclei. Given the importance of septal nuclei for social behaviors, it is somewhat surprising that it has never been investigated whether they are involved in early social responses of naïve animals. In the present study we wanted to know if simple exposure of visually naïve newly hatched chicks to a visual object (an alive, behaving conspecific), that also contains all features to which chicks are known to express early social predispositions, will selectively activate septal areas. We measured brain activity by visualizing the immediate early gene product c‐Fos with a standard immunohistochemical procedure. Notably, after a brief visual exposure to an alive behaving conspecific septum showed higher activation in experimental subjects, compared to baseline animals that were exposed to the same environment in the absence of the conspecific. This is, to the best of our knowledge, the first demonstration of septal involvement in early social responses. We also found similar effects in the nucleus taeniae and arcopallium (amygdala homologues), but not in the medial striatum. This result indicates that at least some nuclei of the social decision making network may participate in early responses to social stimuli. Future studies could capitalize on these results, by identifying the specific visual cues eliciting this effect.

Unsupervised statistical learning in newly hatched chicks

The ability to extract probabilistic information from visual inputs has been reported in human adults and infants (reviewed in [1,2]), and in adults of non-human species, though only under supervised (conditioning) procedures [3]. Here, we report spontaneous sensitivity to the probabilistic structure underlying sequences of visual stimuli in newly hatched domestic chicks using filial imprinting, suggesting that statistical learning may be fully operating at the onset of life in precocial avian species.

Embryonic Exposure to Valproic Acid impairs Social Predispositions for Dynamic Cues of Animate Motion in Newly-Hatched Chicks

Predispositions to preferentially orient towards cues associated with social partners, such as face-like stimuli or biological and animate motion, appear to guide social behavior from the onset of life. These predispositions have been documented in several vertebrate species including human neonates, young monkeys and newly-hatched domestic chicks. Human newborns at high familiar risk of Autism Spectrum Disorder (ASD) show a remarkable deficit in their attention toward these predisposed stimuli, either static and dynamic, compared to newborns at low risk. A previous study showed that prenatal exposure to valproic acid (VPA) (that in humans increases the risk of developing ASD) impairs the chicks’ predisposition to approach naturalistic social stimuli that convey static configurations of features (a stuffed hen), without impairing general cognitive and learning abilities. Here we investigated the effect of VPA exposure on another class of social predispositions, i.e. the spontaneous preference to approach self-propelled objects, namely objects that display autonomous changes in speed. We observed that the preference for stimuli displaying autonomous changes in speed was impaired in VPA-compared to vehicle-injected chicks. Our results indicate an effect of VPA on the development of predisposed orienting mechanisms towards dynamic stimuli, that could be used to investigate the molecular and neurobiological mechanisms underlying ASD early symptoms.

Embryonic Exposure to Valproic Acid Impairs Social Predispositions of Newly-Hatched Chicks

Biological predispositions to attend to visual cues, such as those associated with face-like stimuli or with biological motion, guide social behavior from the first moments of life and have been documented in human neonates, infant monkeys and domestic chicks. Impairments of social predispositions have been recently reported in neonates at high familial risk of Autism Spectrum Disorder (ASD). Using embryonic exposure to valproic acid (VPA), an anticonvulsant associated to increased risk of developing ASD, we modeled ASD behavioral deficits in domestic chicks. We then assessed their spontaneous social predispositions by comparing approach responses to a stimulus containing a face configuration, a stuffed hen, vs. a scrambled version of it. We found that this social predisposition was abolished in VPA-treated chicks, whereas experience-dependent mechanisms associated with filial imprinting were not affected. Our results suggest a specific effect of VPA on the development of biologically-predisposed social orienting mechanisms, opening new perspectives to investigate the neurobiological mechanisms involved in early ASD symptoms.

Visually-naïve chicks prefer agents that move as if constrained by a bilateral body-plan

From the first hours of life, the prompt detection of animate agents allows identification of biologically relevant entities. The motion of most animate agents is constrained by their bilaterally-symmetrical body-plan, and consequently tends to be aligned with the main body-axis. Thus parallelism between the main axis of a moving object and its motion trajectory can signal the presence of animate agents. Here we demonstrated that visually-naïve newborn chicks (Gallus gallus domesticus) are attracted to objects displaying such parallelism, and thus show preference for the same type of motion patterns that elicit perception of animacy in humans. This is the first demonstration of a newborn non-human animals social preference for a visual cue related to the constraints imposed on behaviour by bilaterian morphology. Chicks also showed preference for rotational movements - a potential manifestation of self-propulsion. Results are discussed in relation to the mechanisms of animacy and agency detection in newborn organisms.