Context-Dependent Gestural Laterality: A Multifactorial Analysis in Captive Red-Capped Mangabeys

Catarrhine primates gesture preferentially with their right hands, which led to the hypothesis of a gestural origin of human left-hemispheric specialization for language. However, the factors influencing this gestural laterality remain understudied in non-hominoid species, particularly in intraspecific contexts, although it may bring valuable insights into the proximate and ultimate causes of language lateralization. We present here a preliminary investigation of intraspecific gestural laterality in catarrhine monkeys, red-capped mangabeys (Cercocebus torquatus). We described the spontaneous production of brachio-manual intentional gestures in twenty-five captive subjects. Although we did not evidence any significant gestural lateralization neither at the individual- nor population-level, we found that mangabeys preferentially use their right hands to gesture in negative social contexts, such as aggressions, suggesting an effect of emotional lateralization, and that they adapt to the position of their receiver by preferentially using their ipsilateral hand to communicate. These results corroborate previous findings from ape studies. By contrast, factors related to gesture form and socio-demographic characteristics of signaler and receiver did not affect gestural laterality. To understand better the relationships between gestural laterality and brain lateralization from an evolutionary perspective, we suggest that the gestural communication of other monkey species should be examined with a multifactorial approach.

Developmental Brain Asymmetry. The Good and the Bad Sides

Brain asymmetry is a hallmark of the human brain. Recent studies report a certain degree of abnormal asymmetry of brain lateralization between left and right brain hemispheres can be associated with many neuropsychiatric conditions. In this regard, some questions need answers. First, the accelerated brain asymmetry is programmed during the pre-natal period that can be called “accelerated brain decline clock”. Second, can we find the right biomarkers to predict these changes? Moreover, can we establish the dynamics of these changes in order to identify the right time window for proper interventions that can reverse or limit the neurological decline? To find answers to these questions, we performed a systematic online search for the last 10 years in databases using keywords. Conclusion: we need to establish the right in vitro model that meets human conditions as much as possible. New biomarkers are necessary to establish the “good” or the “bad” borders of brain asymmetry at the epigenetic and functional level as early as possible.

Limb Preference in Animals: New Insights into the Evolution of Manual Laterality in Hominids

Until the 1990s, the notion of brain lateralization—the division of labor between the two hemispheres—and its more visible behavioral manifestation, handedness, remained fiercely defined as a human specific trait. Since then, many studies have evidenced lateralized functions in a wide range of species, including both vertebrates and invertebrates. In this review, we highlight the great contribution of comparative research to the understanding of human handedness’ evolutionary and developmental pathways, by distinguishing animal forelimb asymmetries for functionally different actions—i.e., potentially depending on different hemispheric specializations. Firstly, lateralization for the manipulation of inanimate objects has been associated with genetic and ontogenetic factors, with specific brain regions’ activity, and with morphological limb specializations. These could have emerged under selective pressures notably related to the animal locomotion and social styles. Secondly, lateralization for actions directed to living targets (to self or conspecifics) seems to be in relationship with the brain lateralization for emotion processing. Thirdly, findings on primates’ hand preferences for communicative gestures accounts for a link between gestural laterality and a left-hemispheric specialization for intentional communication and language. Throughout this review, we highlight the value of functional neuroimaging and developmental approaches to shed light on the mechanisms underlying human handedness.

Lessons from behavioral lateralization in olfaction

Sensory information, sampled by sensory organs positioned on each side of the body may play a crucial role in organizing brain lateralization. This question is of particular interest with regard to the growing evidence of alteration in lateralization in several psychiatric conditions. In this context, the olfactory system, an ancient, mostly ipsilateral and well-conserved system across phylogeny may prove an interesting model system to understand the behavioral significance of brain lateralization. Here, we focused on behavioral data in vertebrates and non-vertebrates, suggesting that the two hemispheres of the brain differentially processed olfactory cues to achieve diverse sensory operations, such as detection, discrimination, identification of behavioral valuable cues or learning. These include reports across different species on best performances with one nostril or the other or odorant active sampling by one nostril or the other, depending on odorants or contexts. In some species, hints from peripheral anatomical or functional asymmetry were proposed to explain these asymmetries in behavior. Instigations of brain activation or more rarely of brain connectivity evoked by odorants revealed a complex picture with regards to asymmetric patterns which is discussed with respect to behavioral data. Along the steps of the discussed literature, we propose avenues for future research.

Emotional arousal in 2D versus 3D virtual reality environments

Previous studies have suggested that virtual reality (VR) can elicit emotions in different visual modes using 2D or 3D headsets. However, the effects on emotional arousal by using these two visual modes have not been comprehensively investigated, and the underlying neural mechanisms are not yet clear. This paper presents a cognitive psychological experiment that was conducted to analyze how these two visual modes impact emotional arousal. Forty volunteers were recruited and were randomly assigned to two groups. They were asked to watch a series of positive, neutral and negative short VR videos in 2D and 3D. Multichannel electroencephalograms (EEG) and skin conductance responses (SCR) were recorded simultaneously during their participation. The results indicated that emotional stimulation was more intense in the 3D environment due to the improved perception of the environment; greater emotional arousal was generated; and higher beta (21–30 Hz) EEG power was identified in 3D than in 2D. We also found that both hemispheres were involved in stereo vision processing and that brain lateralization existed in the processing.

The “right” side of sleeping: laterality in resting behaviour of Aldabra giant tortoises (Aldabrachelys gigantea)

Although some studies investigated lateralization in reptiles, little research has been done on chelonians, focusing only on few behaviours such as righting response and escape preference. The aim of this study was to investigate lateralization in Aldabra giant tortoises (Aldabrachelys gigantea), focusing on asymmetrical positioning of the limbs and the head during resting behaviour, called sleep-like behaviour, involving both wild tortoises and individuals under human care. Subjects of the study were 67 adult Aldabra tortoises (54 free ranging on Curieuse, 13 under human care in Mahè Botanical Garden). For each tortoise observed during sleep-like behaviour, we recorded the position of the head (on the left, on the right or in line with the body midline) and we collected which forelimb and hindlimb were kept forward. Moreover, the number of subjects in which limbs were in a symmetrical position during the sleep-like behaviour was recorded. Based on our results, the number of tortoises with asymmetrical position of head and limb was higher (head: 63%; forelimbs: 88%; hindlimbs: 70%) than the number of tortoises with symmetrical position of the head and the limb. Regarding the head, throughout the subjects found with the asymmetrical position of the head during sleep-like behaviour, tortoises positioning the head on the right (42%) were more than those sleeping with the head on the left (21%). We found a relationship between the position of the forelimbs and hindlimbs during sleep-like behaviour. We reported no differences between Mahè (under human care) and Curieuse (wild) tortoises. Findings of this preliminary study underlined traces of group-level lateralization in head positioning during the sleep-like behaviour, possibly due to a left-eye/right-hemisphere involvement in anti-predatory responses and threatening stimuli as reported in reptiles and other vertebrates. This study aims at adding data on brain lateralization, often linked to lateralized behaviours, in reptiles, especially in chelonians.

Brain Laterality Dynamics Support Human Cognition

Hemispheric lateralization constitutes a core architectural principle of human brain organization underlying cognition, often argued to represent a stable, trait-like feature. However, emerging evidence underlines the inherently dynamic nature of brain networks, in which time-resolved alterations in functional lateralization remain uncharted. Integrating dynamic network approaches with the concept of hemispheric laterality, we map the spatiotemporal architecture of whole-brain lateralization in a large sample of high-quality resting-state fMRI data (N=991, Human Connectome Project). We reveal distinct laterality dynamics across lower-order sensorimotor systems and higher-order associative networks. Specifically, we expose two aspects of the laterality dynamics: laterality fluctuations, defined as the standard deviation of laterality time series, and laterality reversal, referring to the number of zero-crossings in laterality time series. These two measures are associated with moderate and extreme changes in laterality over time, respectively. While laterality fluctuations depict positive association with language function and cognitive flexibility, laterality reversal shows a negative association with the same neurocognitive factors. These opposing interactions indicate a dynamic balance between intra- and inter-hemispheric communication, i.e., segregation and integration of information across hemispheres. Furthermore, in their time-resolved laterality index, the default-mode and language networks correlate negatively with visual/sensorimotor and attention networks, indicating flexible while parallel processing capabilities that are linked to better out-of-scanner cognitive performance. Finally, the laterality dynamics correlate with regional metabolism and structural connectivity and showed significant heritability. Our results provide insights into the adaptive nature of the lateralized brain and new perspectives for future studies of human cognition, genetics and brain disorders.