Elisabetta Versace

Forelimb preferences in human beings and other species: multiple models for testing hypotheses on lateralization

Functional preferences in the use of right/left forelimbs are not exclusively present in humans but have been widely documented in a variety of vertebrate and invertebrate species. A matter of debate is whether non-human species exhibit a degree and consistency of functional forelimb asymmetries comparable to human handedness. The comparison is made difficult by the variability in hand use in humans and the few comparable studies conducted on other species. In spite of this, interesting continuities appear in functions such as feeding, object manipulation and communicative gestures. Studies on invertebrates show how widespread forelimb preferences are among animals, and the importance of experience for the development of forelimb asymmetries. Vertebrate species have been extensively investigated to clarify the origins of forelimb functional asymmetries: comparative evidence shows that selective pressures for different functions have likely driven the evolution of human handedness. Evidence of a complex genetic architecture of human handedness is in line with the idea of multiple evolutionary origins of this trait.

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.

Origins of Knowledge: Insights from Precocial Species

Behavioral responses are influenced by knowledge acquired during the lifetime of an individual and by predispositions transmitted across generations. Establishing the origin of knowledge and the role of the unlearned component is a challenging task, given that both learned and unlearned knowledge can orient perception, learning, and the encoding of environmental features since the first stages of life. Ethical and practical issues constrain the investigation of unlearned knowledge in altricial species, including human beings. On the contrary, precocial animals can be tested on a wide range of tasks and capabilities immediately after birth and in controlled rearing conditions. Insects and precocial avian species are very convenient models to dissect the knowledge systems that enable young individuals to cope with their environment in the absence of specific previous experience. We present the state of the art of research on the origins of knowledge that comes from different models and disciplines. Insects have been mainly used to investigate unlearned sensory preferences and prepared learning mechanisms. The relative simplicity of the neural system and fast life cycle of insects make them ideal models to investigate the neural circuitry and evolutionary dynamics of unlearned traits. Among avian species, chicks of the domestic fowl have been the focus of many studies, and showed to possess unlearned knowledge in the sensory, physical, spatial, numerical and social domains. Solid evidence shows the existence of unlearned knowledge in different domains in several species, from sensory and social preferences to the left-right representation of the mental number line. We show how non-mammalian models of cognition, and in particular precocial species, can shed light into the adaptive value and evolutionary history of unlearned knowledge.

Spontaneous generalization of abstract multimodal patterns in young domestic chicks

From the early stages of life, learning the regularities associated with specific objects is crucial for making sense of experiences. Through filial imprinting, young precocial birds quickly learn the features of their social partners by mere exposure. It is not clear though to what extent chicks can extract abstract patterns of the visual and acoustic stimuli present in the imprinting object, and how they combine them. To investigate this issue, we exposed chicks (Gallus gallus) to three days of visual and acoustic imprinting, using either patterns with two identical items or patterns with two different items, presented visually, acoustically or in both modalities. Next, chicks were given a choice between the familiar and the unfamiliar pattern, present in either the multimodal, visual or acoustic modality. The responses to the novel stimuli were affected by their imprinting experience, and the effect was stronger for chicks imprinted with multimodal patterns than for the other groups. Interestingly, males and females adopted a different strategy, with males more attracted by unfamiliar patterns and females more attracted by familiar patterns. Our data show that chicks can generalize abstract patterns by mere exposure through filial imprinting and that multimodal stimulation is more effective than unimodal stimulation for pattern learning.

Large-scale assessment of olfactory preferences and learning in Drosophila melanogaster: behavioral and genetic components.

In the Evolve and Resequence method (E&R), experimental evolution and genomics are combined to investigate evolutionary dynamics and the genotype-phenotype link. As other genomic approaches, this methods requires many replicates with large population sizes, which imposes severe restrictions on the analysis of behavioral phenotypes. Aiming to use E&R for investigating the evolution of behavior in Drosophila, we have developed a simple and effective method to assess spontaneous olfactory preferences and learning in large samples of fruit flies using a T-maze. We tested this procedure on (a) a large wild-caught population and (b) 11 isofemale lines of Drosophila melanogaster. Compared to previous methods, this procedure reduces the environmental noise and allows for the analysis of large population samples. Consistent with previous results, we show that flies have a preference for orange vs. apple odor. With our procedure wild-derived flies exhibit olfactory learning in the absence of previous laboratory selection. Furthermore, we find genetic differences in the olfactory learning with relatively high heritability. We propose this large-scale method as an effective tool for E&R and genome-wide association studies on olfactory preferences and learning.

Newborn chicks show inherited variability in early social predispositions for hen-like stimuli

Predispositions of newborn vertebrates to preferentially attend to living beings and learn about them are pervasive. Their disturbance (e.g. in neonates at risk for autism), may compromise the proper development of a social brain. The genetic bases of such predispositions are unknown. We use the well-known visual preferences of newly-hatched chicks (Gallus gallus) for the head/neck region of the hen to investigate the presence of segregating variation in the predispositions to approach a stuffed hen vs. a scrambled version of it. We compared the spontaneous preferences of three breeds maintained genetically isolated for at least eighteen years while identically raised. Visually-naïve chicks of all breeds (Padovana, Polverara and Robusta maculata) showed the same initial preference for the predisposed stimulus, suggesting that the direction of the initial preference might be genetically fixed. A few minutes later though, striking differences emerged between breeds, which could indicate different strategies of dealing with affiliative objects: while the Polverara breed maintained a constant preference across the entire test, the Padovana and Robusta breeds progressively explored the alternative stimulus more. We hence documented the presence of inherited genetic variability in the expression of early social predispositions in interaction with environmental stimuli.

Naïve Chicks Prefer Hollow Objects.

Biological predispositions influence approach and avoid responses from the time of birth or hatching. Neonates of species that require parental care (e.g. human babies and chicks of the domestic fowl) are attracted by stimuli associated with animate social partners, such as face-like configurations, biological motion and self-propulsion. The property of being filled is used as a cue of animacy by 8-month-old human infants but it is not known whether this reflects the effect of previous experience. We used chicks of the domestic fowl (Gallus gallus) to investigate whether the property of being filled vs. hollow elicits spontaneous or learned preferences. To this aim we tested preferences of naïve and imprinted chicks for hollow and closed cylinders. Contrary to our expectations, we documented an unlearned attraction for hollow stimuli. The preference for hollow stimuli decreased when chicks were imprinted on filled stimuli but did not increase when chicks were imprinted on hollow stimuli, suggesting that hollowness is not crucial to determine affiliative responses for imprinting objects. When chicks were imprinted on occluded stimuli that could be either filled or hollow, the preference for hollow stimuli emerged again, showing that imprinting does not disrupt the spontaneous preference for hollow objects. Further experiments revealed that hollow objects were mainly attractive by means of depth cues such as darker innards, more than as places to hide or as objects with high contrast. Our findings point to predisposed preferences for hollow objects, and suggest that early predispositions might be driven by factors different from animacy cues.

Physiological and behavioral responses in Drosophila melanogaster to odorants present at different plant maturation stages.

The fruit fly Drosophila melanogaster feeds and oviposits on fermented fruit, hence its physiological and behavioral responses are expected to be tuned to odorants abundant during later stages of fruit maturation. We used a population of about two-hundred isogenic lines of D. melanogaster to assay physiological responses (electroantennograms (EAG)) and behavioral correlates (preferences and choice ratio) to odorants found at different stages of fruit maturation. We quantified electrophysiological and behavioral responses of D. melanogaster for the leaf compound β-cyclocitral, as well as responses to odorants mainly associated with later fruit maturation stages. Electrophysiological and behavioral responses were modulated by the odorant dose. For the leaf compound we observed a steep dose-response curve in both EAG and behavioral data and shallower curves for odorants associated with later stages of maturation. Our data show the connection between sensory and behavioral responses and are consistent with the specialization of D. melanogaster on fermented fruit and avoidance of high doses of compounds associated with earlier stages of maturation. Odor preferences were modulated in a non-additive way when flies were presented with two alternative odorants, and combinations of odorants elicited higher responses than single compounds.

Evolutionary compromises to environmental toxins: ammonia and urea tolerance in Drosophila suzukii and Drosophila melanogaster.

The invasive species Drosophila suzukii has evolved morphological and behavioral adaptations to lay eggs under the skin of fresh fruits. This results in severe damage of a wide range of small and stone fruits, thus making this species a serious agricultural and economical threat. Drosophila suzukii females typically lay few eggs per fruit, preferring not infested fruits. Hence larvae are exposed to a reduced amount of nitrogenous waste products. On the contrary, the innocuous Drosophila melanogaster lays eggs on fermented fruits already infested by conspecifics, with larvae developing in a crowded environment characterized by accumulation of nitrogenous waste such as ammonia and urea. Given these differences in oviposition and larval ecological niche, we expected different behavioral and physiological mechanisms in the two species to cope with nitrogenous waste. We investigated the impact of different concentrations of ammonia and urea on fecundity and larval development in both species. Females and larvae of D. suzukii showed a greater sensitivity to high concentration of both compounds, with a dramatic decrease in fecundity and egg viability. To better understand the pathways underlying these differences, we evaluated the effect on ornithine aminotransferase and glutathione-S-transferase, two enzymes involved in nitrogen metabolism and stress response that are expressed during larval development. Under ammonia and urea exposure, the expression of these enzymes was significantly reduced in D. suzukii. The fact that D. suzukii’s shift from rotten to fresh fruit as oviposition and larval substrate resulted in less efficient detoxifying and excretory mechanisms represents a potential approach for its control. Fecundity and larval development are in fact dramatically impaired by nitrogen waste products. These findings can help in planning effective strategies of sustainable pest management that targets both females and larvae.

Positional encoding in cotton-top tamarins (Saguinus oedipus)

Strategies used in artificial grammar learning can shed light into the abilities of different species to extract regularities from the environment. In the A(X)nB rule, A and B items are linked but assigned to different positional categories and separated by distractor items. Open questions are how widespread is the ability to extract positional regularities from A(X)nB patterns, which strategies are used to encode positional regularities and whether individuals exhibit preferences for absolute or relative position encoding. We used visual arrays to investigate whether cotton-top tamarins (Saguinus oedipus) can learn this rule and which strategies they use. After training on a subset of exemplars, half of the tested monkeys successfully generalized to novel combinations. These tamarins discriminated between categories of tokens with different properties (A, B, X) and detected a positional relationship between non-adjacent items even in the presence of novel distractors. Generalization, though, was incomplete, since we observed a failure with items that during training had always been presented in reinforced arrays. The pattern of errors revealed that successful subjects used visual similarity with training stimuli to solve the task, and that tamarins extracted the relative position of As and Bs rather than their absolute position, similarly to what observed in other species. Relative position encoding appears to be the default strategy in different tasks and taxa.