Gestures in human and nonhuman primates

The present article offers a condensed overview, of why a comparative view on gestures in human and nonhuman primates may offer important insights to both: researchers of human as well as of nonhuman primates. It is argued that a comparative view may further contribute to the debate over the evolution of language but that in addition it may also enhance understanding of the relation of language and gesture in humans. The article sketches programmatic issues, which are summarized in the list of framing questions for the workshop and this special issue on “Gestural communication in nonhuman and human primates”; it is aimed to clarify conceptual and methodological prerequisites and to offer points of departure for future comparative research.

The present article offers a condensed overview, of why a comparative view on gestures in human and nonhuman primates may offer important insights to both: researchers of human as well as of nonhuman primates. It is argued that a comparative view may further contribute to the debate over the evolution of language but that in addition it may also enhance understanding of the relation of language and gesture in humans. The article sketches programmatic issues, which are summarized in the list of framing questions for the workshop and this special issue on “Gestural communication in nonhuman and human primates”; it is aimed to clarify conceptual and methodological prerequisites and to offer points of departure for future comparative research.

Research into gestures represents a multifaceted field comprising a wide range of disciplines and research topics, varying methods and approaches, and even different species such as humans, apes and monkeys. The aim of this volume (originally published as a Special Issue of Gesture 5:1/2 (2005)) is to bring together the research in gestural communication in both nonhuman and human primates and to explore the potential of a comparative approach and its contribution to the question of an evolutionary scenario in which gestures play a significant role. The topics covered include the spontaneous natural gesture use in social groups of apes and monkeys, but also during interactions with humans, gestures of preverbal children and their interaction with language, speech-accompanying gestures in humans as well as the use of sign-language in human and nonhuman great apes. It addresses researchers with a background in Psychology, Primatology, Linguistics, and Anthropology, but it might also function as an introduction and a documentation state of the art for a wider less specialised audience which is fascinated by the role gestures might have played in the evolution of human language.

The evolution of human language has been discussed for centuries from different perspectives. Linguistic theory has proposed grammar as a core part of human language that has to be considered in this context. Recent advances in neurosciences have allowed us to take a new neurobiological look on the similarities and dissimilarities of cognitive capacities and their neural basis across both closely and distantly related species. A couple of decades ago, the comparisons were mainly drawn between human and non-human primates, investigating the cytoarchitecture of particular brain areas and their structural connectivity. Moreover, comparative studies were conducted with respect to their ability to process grammars of different complexity. So far the available data suggest that non-human primates are able to learn simple probabilistic grammars, but not hierarchically structured complex grammars. The human brain, which easily learns both grammars, differs from the non-human brain (among others) in how two language-relevant brain regions (Broca's area in the inferior frontal cortex and the superior temporal cortex) are connected structurally by fiber tracts which run dorsally and ventrally in the primate brain. Whether the more dominant dorsal pathway in humans compared to non-human primates is causally related to this behavioral difference is an issue of current debate. Ontogenetic findings suggest at least a correlation between the maturation of the dorsal pathway and the behavior to process syntactically complex structures, although the ultimate causal prove is still not available. Thus, the neural basis of complex grammar processing in humans remains to be defined. More recently it has been reported that songbirds are also able to distinguish between sound sequences reflecting complex grammar. Interestingly, songbirds learn to sing by imitating adult song in a process not unlike language development in children. Moreover, the neural circuits supporting this behavior in songbirds bear anatomical and functional similarities to those in humans. In adult humans the fiber tract connecting the auditory cortex and motor cortex dorsally is known to be involved in the repetition of spoken language. This pathway is present already at birth and is taken to play a major role during language acquisition. In songbirds, detailed information exist concerning the interaction of auditory, motor, and cortical-basal ganglia processing during song learning, and present a rich substrate for comparative studies. The scope of the Research Topic was to bring together contributions of researchers from different fields, who investigate grammar processing in humans, non-human primates, and songbirds with the aim to find answers to the question of what constitutes the neurobiological basis of language and language learning. A number of contributions discuss the ventral and dorsal pathways in human and non-human primates considering their functional roles in speech and language. Some of these take an evolutionary perspective comparing non-human and human primates (Rauschecker, 2012; Rilling et al., 2012), whereas other takes an ontogenetic perspective (Friederici, 2012). The functional roles of the ventral and dorsal pathways in language and other modalities in particular action including articulatory and hand gestures are discussed in further articles (Fitch, 2011; Aboitiz, 2012; Rijntjes et al., 2012). Two articles consider the language system at the interface of two other human specific abilities, namely number processing (Heim et al., 2012) and reading (Lachmann et al., 2012). A couple of contributions take the evolutionary perspective even further by including song birds into their comparative approach (Berwick et al., 2012; Kiggins et al., 2012; Petkov and Jarvis, 2012). The selection of the articles provides a picture of the current views on the evolutionary and neurobiological basis of the language and language learning.

Comparative psychology provides important contributions to our understanding of the origins of human language. The presence of common features in human and nonhuman primate communication can be used to suggest the evolutionary trajectories of potential precursors to language. However, to do so effectively, our findings must be comparable across diverse species. This systematic review describes the current landscape of data available from studies of gestural communication in human and nonhuman primates that make an explicit connection to language evolution. We found a similar number of studies on human and nonhuman primates, but that very few studies included data from more than one species. As a result, evolutionary inferences remain restricted to comparison across studies. We identify areas of focus, bias, and apparent gaps within the field. Different domains have been studied in human and nonhuman primates, with relatively few nonhuman primate studies of ontogeny and relatively few human studies of gesture form. Diversity in focus, methods, and socio-ecological context fill important gaps and provide nuanced understanding, but only where the source of any difference between studies is transparent. Many studies provide some definition for their use of gesture; but definitions of gesture, and in particular, criteria for intentional use, are absent in the majority of human studies. We find systematic differences between human and nonhuman primate studies in the research scope, incorporation of other modalities, research setting, and study design. We highlight eight particular areas in a call to action through which we can strengthen our ability to investigate gestural communication's contribution within the evolutionary roots of human language.

Vocal communication in nonhuman primates receives considerable research attention, with many investigators arguing for similarities between this calling and speech in humans. Data from development and neural organization show a central role of affect in monkey and ape sounds, however, suggesting that their calls are homologous to spontaneous human emotional vocalizations while having little relation to spoken language. Based on this evidence, we propose two principles that can be useful in evaluating the many and disparate empirical findings that bear on the nature of vocal production in nonhuman and human primates. One principle distinguishes production-first from reception-first vocal development, referring to the markedly different role of auditory-motor experience in each case. The second highlights a phenomenon dubbed dual neural pathways, specifically that when a species with an existing vocal system evolves a new functionally distinct vocalization capability, it occurs through emergence of a second parallel neural pathway rather than through expansion of the extant circuitry. With these principles as a backdrop, we review evidence of acoustic modification of calling associated with background noise, conditioning effects, audience composition, and vocal convergence and divergence in nonhuman primates. Although each kind of evidence has been interpreted to show flexible cognitively mediated control over vocal production, we suggest that most are more consistent with affectively grounded mechanisms. The lone exception is production of simple, novel sounds in great apes, which is argued to reveal at least some degree of volitional vocal control. If also present in early hominins, the cortically based circuitry surmised to be associated with these rudimentary capabilities likely also provided the substrate for later emergence of the neural pathway allowing volitional production in modern humans.

Within the evolutionary framework about the origin of human handedness and hemispheric specialization for language, the question of expression of population-level manual biases in nonhuman primates and their potential continuities with humans remains controversial. Nevertheless, there is a growing body of evidence showing consistent population-level handedness particularly for complex manual behaviors in both monkeys and apes. In the present article, within a large comparative approach among primates, we will review our contribution to the field and the handedness literature related to two particular sophisticated manual behaviors regarding their potential and specific implications for the origins of hemispheric specialization in humans: bimanual coordinated actions and gestural communication. Whereas bimanual coordinated actions seem to elicit predominance of left-handedness in arboreal primates and of right-handedness in terrestrial primates, all handedness studies that have investigated gestural communication in several primate species have reported stronger degree of population-level right-handedness compared to noncommunicative actions. Communicative gestures and bimanual actions seem to affect differently manual asymmetries in both human and nonhuman primates and to be related to different lateralized brain substrates. We will discuss (1) how the data of hand preferences for bimanual coordinated actions highlight the role of ecological factors in the evolution of handedness and provide additional support the postural origin theory of handedness proposed by MacNeilage [MacNeilage [2007]. Present status of the postural origins theory. In W. D. Hopkins (Ed.), The evolution of hemispheric specialization in primates (pp. 59-91). London: Elsevier/Academic Press] and (2) the hypothesis that the emergence of gestural communication might have affected lateralization in our ancestor and may constitute the precursors of the hemispheric specialization for language.

Locomotor behavior and control in human and non-human primates: Comparisons with cats and dogs

The aim of my thesis was to investigate how reaching for visual targets placed in 3D space influences the coordinate frames and the kinematics in non-human and human primates. To this end, I conducted three studies. The first study was conducted on non-human primates to find the predominant reference frame of cells in a specific reach related area of the PPC (area PEc) while reaching towards targets placed at different depths and directions; we tested whether PEc reaching cells displayed hand- and/or body-centered coding of reach targets. We found that the majority of PEc neurons encoded targets in a mixed body/hand-centered reference frame. Our findings highlight a role for area PEc as intermediate node between the visually dominated area V6A and the somatosensory dominated area PE. The second study was conducted on healthy human subjects to find the reference frame used while reaching towards targets placed at different depths and directions. Our results revealed reach error patterns based on both eye- and space-centered coordinate systems: in depth more biased towards a space-centered representation and in direction mixed between space- and eye-centered representation. The third study was conducted on a patient with a parietal cortex lesion who showed optic ataxia symptoms. Optic ataxia patients show deficits in visuo-manual guidance especially when reaching to targets located in the periphery of the visual field. By manipulating gaze position and hand position of visual reaching targets, placed at different depth and directions, we investigated how reaching in peripheral and central viewing conditions influenced the trajectories and reach errors of the patient and controls. Our results suggest that the reaching inaccuracies observed, in particular in the configurations where the direction of gaze and reach differed, are due to a disruption of the online correction mechanism and that the PPC is involved in these automatic corrections.

Part 1 Synopsis of the argument: some background information - communication and information, the comparative method - which species to compare and what to conclude?. Part 2 The evolution of communication - historical overview - the design of natural communication systems language evolution - linguists take a look - uniqueness, Noam Chomsky, Derek Bickerton, Philip Lieberman, Charles Hockett, Steven Pinker language evolution - biologists take a look - general comments, Peter Marler, W. John Smith synthesis. Part 3 Conceptual issues in the study of communication: signals designed for a complex environment - the ecology of signal transmission, the ecology of signal detection, adaptation and signal design problems of similarity and classification - the concept of similarity, similarity and classification, units of analysis and their classification in communication potential fruits of Tinbergen's research design. Part 4 Biological design and communication: mating signals - frogs and birds - anuran advertisement calls, avian song survival signals - bats - bat echolocation - the problem social signals - nonhuman and human primates - nonhuman primate vocalisations - general, human language, facial expression and perception in primates. Part 5 Genetic design and communication: mating signals - birds - avian song survival signals - squirrels and primates - ground squirrel alarms, vervet monkey alarm calls social signals - primates - nonhuman primate vocalisations, human spoken language, human sign language, facial and gestural expressions in primates. Part 6 Design and communication: mating signals - frogs, birds, and primates - anuran advertisement calls,, avian advertisement signals, primate copulation calls and sexual swellings survival signals - insects, birds, squirrels, and primates - alarm signals, warning colours, food-associated signals social signals - birds and primates - dominance signals and cues. (Part contents).

Introduction: Gestural communication in nonhuman and human primates

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Gestural Communication in Nonhuman and Human Primates

Vocal communication is common in the animal kingdom. Researchers often examine vocal communication in nonhuman primates (primates) with the aim of identifying similarities and differences with human language and speech, in order to trace the evolutionary origins of our complex communication system. Primates can produce distinct calls in response to specific events, such as the discovery of a certain predator, and listeners seem to understand what these calls refer to. Although on the surface there are similarities between this type of communication and human referential words, the mental processes that underlie them may be very different. While in general the flexibility shown by primate receivers may demonstrate some commonalities with humans, there is much more controversy over whether there are similarities between the production of primate vocalizations and language. It is widely accepted that primates, unlike humans, lack the ability to generate new vocalizations. Although this means primates have a closed repertoire of calls that cannot be expanded, primates are capable of combining their existing calls to generate new messages. The degree of voluntary control and intentionality involved in the use of calls is also a matter of debate, with recent evidence on both a neural and behavioral level challenging traditional assumptions that primate vocalizations are used in an automatic, reflexive manner. More research is needed to examine the mental processes underlying communicative behavior in both the producer and the receiver. In the future adopting a more holistic, multimodal approach to studying primate communication is likely to challenge and ultimately improve our understanding of primate communication and the evolution of human language.

Comparative research on communication systems in human and non-human primates has struggled to find a common language for comparisons. Research has too often either embraced application of linguistic constructs to animal signals, or eschewed them altogether, with the result being either uncritical acceptance of continuity between human and animal communication, or wholesale dismissal of it. This chapter attempts to better align the discussion of communication in the two groups by highlighting the importance of low-level features of communication indisputably common to both. From this common starting point, the authors of this chapter invoke functional deployability as a critical pressure influencing signal structure and use, emphasizing conserved perceptuocognitive mechanisms as common targets of signal action. In recognizing these foundational building blocks, many productive avenues for future research open up. In particular, the authors suggest that perceptual and cognitive biases that promote certain types of signal-meaning mappings provide a natural, biosemantic substrate on which more robust communicative systems can be built.