Gillian S. Forrester

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.

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.

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.

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.

A multidimensional approach to investigations of behaviour: revealing structure in animal communication signals

Studies of animal behaviour reveal that some species havecognitive skills once believed to be evolutionary adapta-tions unique to humans (e.g. tool use, cooperative hunt-ing; e.g. Boesch & Boesch 1989; Stanford et al. 1994;Boesch 2001). However, our ability to comprehend andgenerate spontaneous and novel phrases with underlyingsemantic and syntactic structure still sets us apart fromother animal species. Research suggests that the abilityto acquire and use human language is linked to the evolu-tion of specific increased neocortical volume (Barton DHauser 1996). However, exactly how modern human lan-guage evolved from our preverbal communication skills isstill poorly understood.It has long been accepted that communication is a pro-cess in which animals use their sensory organs to send andreceive information about the world (Darwin 1872; Tin-bergen 1959; Marler 1965). Humans use a rich repertoireof verbal and nonverbal signals to communicate. Alongwith the salient auditory signal of vocal speech, we use vi-sual communication signals in the form of manual ges-tures, body postures, facial expressions and eye gaze,which are important for providing information about in-dividual identity, social hierarchy, emotional states, inten-tions and receptiveness (Tomasello & Camaioni 1997).Like humans, many animal species produce and respondto information in the surrounding environment with sig-nals comprising combinations of sensory components.These signals are considered to be ‘multimodal’ or ‘multi-sensory’ (Ho¨lldobler 1995; Johnstone 1995, 1996). Forinstance, in humans, facial expression and visual articula-tory movements play a role in vocal perception (McGurk& Macdonald 1976; Smith 1977, 1990; Massaro 1998).Qualitative analyses of communication suggest thatsignalling is not only a multisensory process, but also adynamic one that is greatly influenced by contextualfactors (King & Shanker 2003).Evidence from various animal studies has demonstratedthe presence of signal structure during communication.These species include the honeybee, Apis mellifera (vonFrisch 1947, 1967; Seeley 1995; Dornhaus & Chittka1999), Gunnison’s prairie dog, Cynomys gunnisoni (Slobod-chikoff et al. 1991; Slobodchikoff & Placer 2006), suri-cates, Suricata suricatta (Manser 2001; Manser et al. 2001)and several species of birds, including fowl, Gallus gallus(Evans et al. 1993; Evans & Marler 1994; Evans & Evans1999), ravens, Corvus corax (Bugnyar et al. 2001), yellowwarblers, Dendroica petechia (Gill & Sealy 2004) andblack-capped chickadees, Poecile atricapilla (Templetonet al. 2005). Semantic or referential structure in animalcommunication is important because it allows scientiststo draw parallels between animal communication and hu-man language (Hauser 1996; Evans 1997; Fitch 2005).Communication research suggests that some nonhumanprimates can produce alarm calls with semantic structure(Chlorocebus aethiops: Seyfarth et al. 1980a; Macaca mu-latta: Marler et al. 1992; Cercopithecus diana: Zuberbu¨hleret al. 1997; Zuberbu¨hler 2000a). Some species can responddifferentially to vocalizations based on the informationthey provide (C. aethiops: Seyfarth et al. 1980b; Chlorocebus

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.

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.

Structured bimanual actions and hand transfers reveal population-level right-handedness in captive gorillas

There is a common prevailing perception that humans possess a species-unique population-level right-hand bias that has evolutionary links with language. New theories suggest that an early evolutionary division of cognitive function gave rise to a left-hemisphere bias for behaviours underpinned by structured sequences of actions. However, studies of great ape handedness have generated inconsistent results and considerable debate. Additionally, the literature places a heavy focus on chimpanzees, revealing a paucity of handedness findings from other great ape species, and thus limiting the empirical evidence with which we can evaluate evolutionary theory. We observed handedness during spontaneous naturalistic bimanual actions in a captive, biological group of 13 western lowland gorillas, Gorilla gorilla gorilla. Our results demonstrated a significant group-level right-handed bias for bimanual actions as well as for a novel measure of handedness: hand transfer. The two measures revealed similar patterns of handedness, such that a right-hand bias for the majority of individuals was found across both measures. Our findings suggest that human population-level right-handedness is a behavioural trait linked with left-hemisphere dominance for the processing of structured sequences of actions, and was inherited by a common ancestor of both humans and apes.

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.

The right hand man: manual laterality and language

Investigations of human laterality suggest motor preference is not arbitrary, but rather represents an evolutionary bias stemming from the asymmetric organization of underlying neural function for skilled action. The most prominent manifestation of lateralized motor behavior in humans is right-handedness. While human right-handedness provides a highly reliable marker for the brain organization of left hemisphere language function, the causal evolutionary link between the two remains highly controversial. Once considered a unique hallmark of human evolution, structural neuroanatomical investigations have now revealed homologous asymmetric language regions (larger left hemisphere) in great apes, providing evidence for a common mechanism underlying communication processes in humans and apes. However, whether this translates into a handedness bias in great apes remains highly controversial. This chapter discusses the unique characteristics of human and non-human primate handedness within an evolutionary framework and explores new manual laterality findings, celebrating the emergence of multimodal, quantitative methodologies aimed at bridging the gap between studies of brain and behavior.