Social gaze in preterm infants may act as an early indicator of atypical lateralization.

Visual field biases have been identified as markers of atypical lateralization in children with developmental conditions, but this is the first investigation to consider early lateralized gaze behaviors for social stimuli in preterm infants. Eye-tracking methods with 51 preterm (33 male, 92.1% White) and 61 term-born (31 male, 90.1% White) infants aged 8-10 months from Edinburgh, UK, captured the development of visual field biases, comparing gaze behavior to social and non-social stimuli on the left versus right of the screen. Preterm infants showed a significantly reduced interest to social stimuli on the left versus right compared to term children (d = .58). Preterm children exhibit early differential orienting preferences that may be an early indicator of atypical lateralized function.

Hindsight 20/20: The future of laterality research.

The last decade of laterality research has been bolstered by a significant broadening in theoretical framing and investigative approaches. Comparative research contributions continue to strengthen the position that ancient functional and anatomical brain biases are preserved in modern humans. However, how they unfold over developmental time and contribute to cognitive abilities is still unclear. To make further advances, we must position human brains and behaviors within an evolutionary framework. This includes viewing motor-sensory behavior as an integral part of a developing cognitive system.

An analysis of bimanual actions in natural feeding of semi-wild chimpanzees.

OBJECTIVE: The objective of the current study was to investigate the lateral dominance for a bimanually coordinated natural feeding behavior in semi-wild chimpanzees. METHODS: Strychnos spp. fruit consumption behaviors in semi-wild chimpanzees as an ecologically comparable feeding behavior to those found in cerebral lateralization studies of non-primate species was investigated. Video recordings of 33 chimpanzees were assessed while they consumed hard-shelled strychnos fruits. Statistical and descriptive measures of hand dominance to highlight lateralized patterns were explored. RESULTS: Statistical evaluation of feeding bouts revealed a group-level right-handed bias for bimanual coordinated feeding actions, however, few individuals were statistically lateralized. Descriptive analyses revealed that the majority of individuals were lateralized and possessed a right-handed bias for strychnos feeding behavior. CONCLUSIONS: The results provided empirical evidence in support of an early evolutionary delineation of function for the right and left hemispheres. The present findings suggest that great apes express an intermediate stage along the phylogenetic trajectory of human manual lateralization.

Social environment elicits lateralized navigational paths in two populations of typically developing children.

The current study provides the first evidence of human lateralized navigation of a social space within a naturalistic environment. We employed a quantitative, observational approach and report on a detailed set of nearly 700 independent navigational routes from two separate child populations consisting of over 300 typically developing children, aged five to fourteen years. The navigational path was considered across the sagittal plane (left, right) around three distinct target types (peer, adult and object). Both child populations expressed a significant bias for choosing a rightward navigational path around a human target (e.g., peer, adult) and no lateral preference for navigation around fixed, inanimate objects. A rightward navigational path provides an advantage for the left visual field and the right hemisphere, facilitating both the production and perception of social-emotion stimuli. The findings are consistent with evidence from studies of non-human animal species demonstrating that the social environment elicits predictable lateralized behavior, and support an early evolutionary delineation of functional processing by the two hemispheres.

Motor-sensory biases are associated with cognitive and social abilities in humans.

Across vertebrates, adaptive behaviors, like feeding and avoiding predators, are linked to lateralized brain function. The presence of the behavioral manifestations of these biases are associated with increased task success. Additionally, when an individual's direction of bias aligns with the majority of the population, it is linked to social advantages. However, it remains unclear if behavioral biases in humans correlate with the same advantages. This large-scale study (N = 313-1661, analyses dependent) examines whether the strength and alignment of behavioral biases associate with cognitive and social benefits respectively in humans. To remain aligned with the animal literature, we evaluate motor-sensory biases linked to motor-sequencing and emotion detection to assess lateralization. Results reveal that moderate hand lateralization is positively associated with task success and task success is, in turn, associated with language fluency, possibly representing a cascade effect. Additionally, like other vertebrates, the majority of our human sample possess a 'standard' laterality profile (right hand bias, left visual bias). A 'reversed' profile is rare by comparison, and associates higher self-reported social difficulties and increased rate of autism and/or attention deficit hyperactivity disorder. We highlight the importance of employing a comparative theoretical framing to illuminate how and why different laterization profiles associate with diverging social and cognitive phenotypes.

Target animacy influences chimpanzee handedness.

We employed a bottom-up, quantitative method to investigate great ape handedness. Our previous investigation of gorillas (Gorilla gorilla gorilla) demonstrated that contextual information influenced an individual's handedness toward target objects. Specifically, we found a significant right-hand bias for unimanual actions directed toward inanimate target objects but not for actions directed to animate target objects (Forrester et al. in Anim Cogn 14(6):903-907, 2011). Using the identical methodological technique, we investigated the spontaneous hand actions of nine captive chimpanzees (Pan troglodytes) during naturalistic, spontaneous behavior. We assessed both the frequencies and proportions of lateralized hand actions directed toward animate and inanimate targets employing focal follow video sampling. Like the gorillas, the chimpanzees demonstrated a right-handed bias for actions directed toward inanimate targets, but not toward animate targets. This pattern was evident at the group level and for the majority of subjects at the individual level. We postulate that a right-hand bias for only inanimate targets reflects the left hemisphere's dominant neural processing capabilities for objects that have functional properties (inanimate objects). We further speculate that a population-level right-hand bias is not a human-unique characteristic, but one that was inherited from a common human-ape ancestor.

Target animacy influences gorilla handedness.

We investigated the unimanual actions of a biological family group of twelve western lowland gorillas (Gorilla gorilla gorilla) using a methodological approach designed to assess behavior within social context from a bottom-up perspective. Measures of both the lateralization of unimanual actions (left, right) and the target of the action (animate, inanimate) were assessed during dual, synchronized video observations of naturalistic behavior. This paper demonstrates a corelationship between handedness and the animate quality of the target object. Analyses demonstrated a significant interaction between lateralized unimanual actions and target animacy and a right-hand bias for actions directed toward inanimate targets. We suggest that lateralized motor preference reflects the different processing capabilities of the left and right hemispheres, as influenced by the emotive (animate) and/or functional (inanimate) characteristics of the target, respectively.

Gaze behaviour to lateral face stimuli in infants who do and do not gain an ASD diagnosis.

Cerebral lateralisation of function is common characteristic across vertebrate species and is positively associated with fitness of the organism, in humans we hypothesise that it is associated with cognitive fitness. This investigation evaluated the early development of lateralised gaze behaviour for face stimuli in infants at high and low risk for autism from the British Autism Sibling Infant Study (BASIS). The BASIS cohort includes a low risk group and three high-risk groups who at age 3 were developing (i) typically, (ii) atypically or (iii) had received a diagnosis for ASD. Using eye-tracking data derived from a face pop-out task at 6 and 14 months of age, all non-ASD groups showed a bias for stimuli on the left at both timepoints. At 6 months the ASD group demonstrated a preference for stimuli on the right and were slower than their neurotypical counterparts to look at faces on the left. However, by 14 months these differences disappear. Longitudinal associations between lateral looking behaviour at 6 months and language and motor ability at 14 months were also found. Results suggest that infants who go on to be diagnosed with autism exhibit early differences in gaze behaviour that may be associated with subsequent cognitive outcomes.

Author Correction: Gaze behaviour to lateral face stimuli in infants who do and do not receive an ASD diagnosis.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Evolutionary motor biases and cognition in children with and without autism.

Evolution has endowed vertebrates with a divided brain that allows for processing of critical survival behaviours in parallel. Most humans possess a standard functional brain organisation for these ancient sensory-motor behaviours, favouring the right hemisphere for fight-or-flight processes and the left hemisphere for performing structured motor sequences. However, a significant minority of the population possess an organisational phenotype that represents crowding of function in one hemisphere, or a reversal of the standard functional organisation. Using behavioural biases as a proxy for brain organisation, results indicate that reversed brain organisation phenotype increases in populations with autism and is associated with weaker cognitive abilities. Moreover, this study revealed that left-handedness, alone, is not associated with decreased cognitive ability or autism. Rather, left-handedness acts as a marker for decreased cognitive performance when paired with the reversed brain phenotype. The results contribute to comparative research suggesting that modern human abilities are supported by evolutionarily old, lateralised sensory-motor processes. Systematic, longitudinal investigations, capturing genetic measures and brain correlates, are essential to reveal how cognition emerges from these foundational processes. Importantly, strength and direction of biases can act as early markers of brain organisation and cognitive development, leading to promising, novel practices for diagnoses and interventions.

Received Cradling Bias During the First Year of Life: A Retrospective Study on Children With Typical and Atypical Development.

A population-level left cradling bias exists whereby 60-90% of mothers hold their infants on the left side. This left biased positioning appears to be mutually beneficial to both the mother and the baby's brain organization for processing of socio-emotional stimuli. Previous research connected cradling asymmetries and Autism Spectrum Disorders (ASD), entailing impairment in socio-communicative relationships and characterized by an early hypo-lateralization of brain functions. In this explorative study, we aimed to provide a contribution to the retrospective investigations by looking for early behavioral markers of neurodevelopmental disorders such as ASD. We hypothesized that an atypical trajectory in maternal cradling might be one of the possible signs of an interference in mother-infant socio-emotional communication, and thus of potential neurodevelopmental dysfunctions. To this aim, we examined photos depicting mother-child early cradling interactions by consulting family albums of 27 children later diagnosed with ASD and 63 typically developing children. As regards the first half of the first year of life, no differences were shown between maternal cradling-side preferences in typical and ASD groups, both exhibiting the left-cradling bias in the 0-3 months period, but not in the 3-6 months period. However, our results show dissimilar patterns of cradling preferences during the second half of the first year of life. In particular, the absence of left-cradling shown in typical mothers was not observed in ASD mothers, who exhibited a significant left-cradling bias in the 6-12 months age group. This difference might reflect the fact that mother-infant relationship involving children later diagnosed with ASD might remain "basic" because mothers experience a lack of social activity in such children. Alternatively, it may reflect the overstimulation in which mothers try to engage infants in response to their lack of responsiveness and social initiative. However, further investigations are needed both to distinguish between these two possibilities and to define the role of early typical and reversed cradling experiences on neurodevelopment.

The left cradling bias: An evolutionary facilitator of social cognition?

A robust left side cradling bias (LCB) in humans is argued to reflect an evolutionarily old left visual field bias and right hemisphere dominance for processing social stimuli. A left visual field bias for face processing, invoked via the LCB, is known to reflect a human population-level right cerebral hemisphere specialization for processing social stimuli. We explored the relationship between cradling side biases, hand dominance and socio-communicative abilities. Four and five year old typically-developing children (N = 98) participated in a battery of manual motor tasks interspersed by cradling trials comprising a(n): infant human doll, infant primate doll, proto-face pillow and no-face pillow. Mean social and communication ability scores were obtained via a survey completed by each child's key teacher. We found a population-level LCB for holding an infant human doll that was not influenced by hand dominance, sex, age or experience of having a younger sibling. Children demonstrating a LCB, did however, obtain a significantly higher mean social ability score compared with their right side cradling counterparts. Like the infant human doll, the proto-face pillow's schematic face symbol was sufficient to elicit a population-level LCB. By contrast, the infant primate doll elicited a population-level right side cradling bias, influenced by both hand dominance and sex. The findings suggest that the LCB is present and visible early in development and is likely therefore, to represent evolutionarily old domain-specific organization and function of the right cerebral hemisphere. Additionally, results suggest that a LCB requires minimal triggering but can be reversed in some situations, possibly in response to species-type or levels of novelty or stress as perceived by the viewer. Patterns of behavioral biases within the context of social stimuli and their associations with cognitive ability are important for understanding how socio-communication abilities emerge in developing children.

A comparative perspective on lateral biases and social behavior.

Cerebral lateralization and associated motor behaviors were historically thought to be characteristics unique to humans. Today, it is clear that these features are present and visible in other animal species. These shared attributes of brain and behavior suggest inheritance from a distant common ancestor. Population-level motor biases are likely to reflect an early evolutionary division of primary survival functions of the brain's left and right hemispheres. In modern humans, these features may provide a foundational platform for the development of higher cognitive functions, inextricably cementing the ties between the evolution and development of cognition. This chapter focuses on the links between a vertebrate-wide right hemisphere dominance for perceiving and producing social signals, left side motor biases (inclusive of visual field preferences), and the evolution and development of cognition in modern humans.

Slip of the tongue: Implications for evolution and language development.

A prevailing theory regarding the evolution of language implicates a gestural stage prior to the emergence of speech. In support of a transition of human language from a gestural to a vocal system, articulation of the hands and the tongue are underpinned by overlapping left hemisphere dominant neural regions. Behavioral studies demonstrate that human adults perform sympathetic mouth actions in imitative synchrony with manual actions. Additionally, right-handedness for precision manual actions in children has been correlated with the typical development of language, while a lack of hand bias has been associated with psychopathology. It therefore stands to reason that sympathetic mouth actions during fine precision motor action of the hands may be lateralized. We employed a fine-grained behavioral coding paradigm to provide the first investigation of tongue protrusions in typically developing 4-year old children. Tongue protrusions were investigated across a range of cognitive tasks that required varying degrees of manual action: precision motor action, gross motor action and no motor actions. The rate of tongue protrusions was influenced by the motor requirements of the task and tongue protrusions were significantly right-biased for only precision manual motor action (p<.001). From an evolutionary perspective, tongue protrusions can drive new investigations regarding how an early human communication system transitioned from hand to mouth. From a developmental perspective, the present study may serve to reveal patterns of tongue protrusions during the motor development of typically developing children.

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 preference 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 evolutionary adaptive value of social stimulus as a triggering factor for the manifestation of group-level lateralized behaviors.

Handedness as a marker of cerebral lateralization in children with and without autism.

We employed a multiple case studies approach to investigate lateralization of hand actions in typically and atypically developing children between 4 and 5 years of age. We report on a detailed set of over 1200 hand actions made by four typically developing boys and four boys with autism. Participants were assessed for unimanual hand actions to both objects and the self (self-directed behaviors). Individual and group analyses suggest that typically developing children have a right hand dominance for hand actions to objects and a left hand dominance for hand actions for self-directed behaviors, revealing a possible dissociation for functional specialization of the left and right hemispheres respectively. Children with autism demonstrated mixed-handedness for both target conditions, consistent with the hypothesis that there is reduced cerebral specialization in these children. The findings are consistent with the view that observed lateralized motor action can serve as an indirect behavioral marker for evidence of cerebral lateralization.

Human handedness: an inherited evolutionary trait.

Our objective was to demonstrate that human population-level, right-handedness, is not species specific, precipitated from language areas in the brain, but rather is context specific and inherited from a behavior common to both humans and great apes. In general, previous methods of assessing human handedness have neglected to consider the context of action, or employ methods suitable for direct comparison across species. We employed a bottom-up, context-sensitive method to quantitatively assess manual actions in right-handed, typically developing children during naturalistic behavior. By classifying the target to which participants directed a manual action, as animate (social partner, self) or inanimate (non-living functional objects), we found that children demonstrated a significant right-hand bias for manual actions directed toward inanimate targets, but not for manual actions directed toward animate targets. This pattern was revealed at both the group and individual levels. We used a focal video sampling, corpus data-mining approach to allow for direct comparisons with captive gorillas (Forrester et al. Animal Cognition 2011;14(6):903-7) and chimpanzees (Forrester et al. Animal Cognition, in press). Comparisons of handedness patters support the view that population-level, human handedness, and its origin in cerebral lateralization is not a new or human-unique characteristic. These data are consistent with the theory that human right-handedness is a trait developed through tool use that was inherited from an ancestor common to both humans and great apes.