Social environment elicits lateralized behaviors in Gorillas (Gorilla gorilla gorilla) and Chimpanzees (Pan troglodytes)

The influence of the social environment on lateralized behaviors has now been investigated across a wide variety of animal species. New evidence suggests that the social environment can modulate behavior. Currently, there is a paucity of data relating to how primates navigate their environmental space, and investigations that consider the naturalistic context of the individual are few and fragmented. Moreover, there are competing theories about whether only the right or rather both cerebral hemispheres are involved in the processing of social stimuli, especially in emotion processing. Here we provide the first report of lateralized social behaviors elicited by great apes. We employed a continuous focal animal sampling method to record the spontaneous interactions of a captive zoo-living colony of chimpanzees (Pan troglodytes) and a biological family group of peer-reared western lowland gorillas (Gorilla gorilla gorilla). We specifically focused on which side of the body (i.e., front, rear, left, right) the focal individual preferred to keep conspecifics. Utilizing a newly developed quantitative corpus-coding scheme, analysis revealed both chimpanzees and gorillas demonstrated a significant group-level prefer- ence for focal individuals to keep conspecifics positioned to the front of them compared with behind them. More interestingly, both groups also manifested a population-level bias to keep conspecifics on their left side compared with their right side. Our findings suggest a social processing dominance of the right hemisphere for context-specific social environments. Results are discussed in light of the evolu- tionary adaptive value of social stimulus as a triggering factor for the manifestation of group-level lateralized behaviors

Effects of oxytocin-family peptides and substance P on locomotor activity and filial preferences in visually naïve chicks.

Nonapeptides from the vasopressin/oxytocin family have been implicated in a wide variety of social behaviors across vertebrates. Experimental manipulations that alter nonapeptide levels or receptor function in the brain have provided evidence for understanding how nonapeptides influence responses to social stimuli in adults. While behaviors in adults have been extensively studied, much less in known about roles of nonapeptides in early life and the development of affiliative social behaviors. We examined an experience-independent preference (social predisposition) that is present at hatching and is characterized by the tendency of visually naïve chicks (Gallus gallus) to prefer to approach a stuffed-hen stimulus over a control stimulus in a choice test. Among chicks that show the social predisposition preference, bilateral intracranial mesotocin injections resulted in higher mean hen preference scores compared to saline-injected controls. Equimolar doses of mesotocin and vasotocin injections had different effects on locomotor activity: vasotocin, but not mesotocin, resulted in hypoactivity. We also tested whether intraperitoneal substance P had an effect on hen preference scores because previous research has proposed that vasotocin effects on social approach are mediated by peripheral release of substance P, but found no significant effect. All together, our data suggests that mesotocin signaling may be important for social predispositions and can potentially enhance the perceived salience of social stimuli soon after hatching. Specifically, mesotocin release and signaling in the brain may regulate the ability to recognize naturalistic stimuli and/or to act on the motivation to approach naturalistic stimuli

Numerical magnitude, rather than individual bias, explains spatial numerical association in newborn chicks

We associate small numbers with the left and large numbers with the right side of space. Recent evidence from human newborns and non-human animals has challenged the primary role assigned to culture, in determining this spatial numerical association (SNA). Nevertheless, the effect of individual spatial biases has not been considered in previous research. Here, we tested the effect of numerical magnitude in SNA and we controlled for itablendividual biases. We trained 3-day-old chicks (Gallus gallus) on a given numerical magnitude (5). Then chicks could choose between two identical, left or right, stimuli both representing either 2, 8, or 5 elements. We computed the percentage of Left-sided Choice (LC). Numerical magnitude, but not individual lateral bias, explained LC: LC2 vs. 2>LC5 vs. 5>LC8 vs. 8. These findings suggest that SNA originates from pre-linguistic precursors, and pave the way to the investigation of the neural correlates of the number space association

A mental number line in human newborns

Humans represent numbers on a mental number line with smaller numbers on the left and larger numbers on the right side. A left\u2010to\u2010right oriented spatial\u2013numerical association, (SNA), has been demonstrated in animals and infants. However, the possibility that SNA is learnt by early exposure to caregivers\u2019 directional biases is still open. We conducted two experiments: in Experiment 1, we tested whether SNA is present at birth and in Experiment 2, we studied whether it depends on the relative rather than the absolute magnitude of numerousness. Fifty\u2010five\u2010hour\u2010old newborns, once habituated to a number (12), spontaneously associated a smaller number (4) with the left and a larger number (36) with the right side (Experiment 1). SNA in neonates is not absolute but relative. The same number (12) was associated with the left side rather than the right side whenever the previously experienced number was larger (36) rather than smaller (4) (Experiment 2). Control on continuous physical variables showed that the effect is specific of discrete magnitudes. These results constitute strong evidence that in our species SNA originates from pre\u2010linguistic and biological precursors in the brain

Brain and Behavioral Asymmetry: A Lesson From Fish.

It is widely acknowledged that the left and right hemispheres of human brains display both anatomical and functional asymmetries. For more than a century, brain and behavioral lateralization have been considered a uniquely human feature linked to language and handedness. However, over the past decades this idea has been challenged by an increasing number of studies describing structural asymmetries and lateralized behaviors in non-human species extending from primates to fish. Evidence suggesting that a similar pattern of brain lateralization occurs in all vertebrates, humans included, has allowed the emergence of different model systems to investigate the development of brain asymmetries and their impact on behavior. Among animal models, fish have contributed much to the research on lateralization as several fish species exhibit lateralized behaviors. For instance, behavioral studies have shown that the advantages of having an asymmetric brain, such as the ability of simultaneously processing different information and perform parallel tasks compensate the potential costs associated with poor integration of information between the two hemispheres thus helping to better understand the possible evolutionary significance of lateralization. However, these studies inferred how the two sides of the brains are differentially specialized by measuring the differences in the behavioral responses but did not allow to directly investigate the relation between anatomical and functional asymmetries. With respect to this issue, in recent years zebrafish has become a powerful model to address lateralization at different level of complexity, from genes to neural circuitry and behavior. The possibility of combining genetic manipulation of brain asymmetries with cutting-edge in vivo imaging technique and behavioral tests makes the zebrafish a valuable model to investigate the phylogeny and ontogeny of brain lateralization and its relevance for normal brain function and behavior

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

This work was supported by a grant from the European Research Council under the European Union’s Seventh Framework Programme (FP7/2007-2013) Grant ERC-2011-ADG_20110406, Project No: 461 295517, PREMESOR to G.V. Support from Fondazione Caritro Grant Biomarker DSA [40102839] and PRIN 2015 (Neural bases of animacy detection, and their relevance to the typical and atypical development of the brain) to GV is also acknowledged

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

Survival with an Asymmetrical Brain: Advantages and disadvantages of cerebral lateralization

Recent evidence in natural and semi-natural settings has revealed a variety of left-right perceptual asymmetries among vertebrates. These include preferential use of the left or right visual hemifield during activities such as searching for food, agonistic responses, or escape from predators in animals as different as fish, amphibians, reptiles, birds, and mammals. There are obvious disadvantages in showing such directional asymmetries because relevant stimuli may be located to the animal's left or right at random; there is no a priori association between the meaning of a stimulus (e.g., its being a predator or a food item) and its being located to the animal’s left or right. Moreover, other organisms (e.g., predators) could exploit the predictability of behavior that arises from population level lateral biases. It might be argued that lateralization of function enhances cognitive capacity and efficiency of the brain, thus counteracting the ecological disadvantages of lateral biases in behavior. However, such an increase in brain efficiency could be obtained by each individual being lateralized without any need to align the direction of the asymmetry in the majority of the individuals of the population.Here we argue that the alignment of the direction of behavioral asymmetries at the population level arises as an "evolutionarily stable strategy" under "social" pressures occurring when individually asymmetrical organisms must coordinate their behavior with the behavior of other asymmetrical organisms of the same or different species

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