Publications

Abstract

Dance is an icon of human expression. Despite astounding diversity around the world’s cultures and dazzling abundance of reminiscent animal systems, the evolution of dance in the human clade remains obscure. Dance requires individuals to interactively synchronize their whole-body tempo to their partner’s, with near-perfect precision. This capacity is motorically-heavy, engaging multiple neural circuitries, but also dependent on an acute socio-emotional bond between partners. Hitherto, these factors helped explain why no dance forms were present amongst nonhuman primates. Critically, evidence for conjoined full-body rhythmic entrainment in great apes that could help reconstruct possible proto-stages of human dance is still lacking. Here, we report an endogenously-effected case of ritualized dance-like behaviour between two captive chimpanzees – synchronized bipedalism. We submitted video recordings to rigorous time-series analysis and circular statistics. We found that individual step tempo was within the genus’ range of “solo” bipedalism. Between-individual analyses, however, revealed that synchronisation between individuals was non-random, predictable, phase concordant, maintained with instantaneous centi-second precision and jointly regulated, with individuals also taking turns as “pace-makers”. No function was apparent besides the behaviour’s putative positive social affiliation. Our analyses show a first case of spontaneous whole-body entrainment between two ape peers, thus providing tentative empirical evidence for phylogenies of human dance. Human proto-dance, we argue, may have been rooted in mechanisms of social cohesion among small groups that might have granted stress-releasing benefits via gait-synchrony and mutual-touch. An external sound/musical beat may have been initially uninvolved. We discuss dance evolution as driven by ecologically-, socially- and/or culturally-imposed “captivity”.

Abstract

We contrast two related hypotheses of the evolution of dance: H1: Maternal bipedal walking influenced the fetal experience of sound and associated movement patterns; H2: The human transition to bipedal gait produced more isochronous/predictable locomotion sound resulting in early music-like behavior associated with the acoustic advantages conferred by moving bipedally in pace. The cadence of walking is around 120 beats per minute, similar to the tempo of dance and music. Human walking displays long-term constancies. Dyads often subconsciously synchronize steps. The major amplitude component of the step is a distinctly produced beat. Human locomotion influences, and interacts with, emotions, and passive listening to music activates brain motor areas. Across dance-genres the footwork is most often performed in time to the musical beat. Brain development is largely shaped by early sensory experience, with hearing developed from week 18 of gestation. Newborns reacts to sounds, melodies, and rhythmic poems to which they have been exposed in utero. If the sound and vibrations produced by footfalls of a walking mother are transmitted to the fetus in coordination with the cadence of the motion, a connection between isochronous sound and rhythmical movement may be developed. Rhythmical sounds of the human mother locomotion differ substantially from that of nonhuman primates, while the maternal heartbeat heard is likely to have a similar isochronous character across primates, suggesting a relatively more influential role of footfall in the development of rhythmic/musical abilities in humans. Associations of gait, music, and dance are numerous. The apparent absence of musical and rhythmic abilities in nonhuman primates, which display little bipedal locomotion, corroborates that bipedal gait may be linked to the development of rhythmic abilities in humans. Bipedal stimuli in utero may primarily boost the ontogenetic development. The acoustical advantage hypothesis proposes a mechanism in the phylogenetic development.

Abstract

Time is one crucial dimension conveying information in animal communication. Evolution has shaped animals’ nervous systems to produce signals with temporal properties fitting their socio-ecological niches. Many quantitative models of mechanisms underlying rhythmic behaviour exist, spanning insects, crustaceans, birds, amphibians, and mammals. However, these computational and mathematical models are often presented in isolation. Here, we provide an overview of the main mathematical models employed in the study of animal rhythmic communication among conspecifics. After presenting basic definitions and mathematical formalisms, we discuss each individual model. These computational models are then compared using simulated data to uncover similarities and key differences in the underlying mechanisms found across species. Our review of the empirical literature is admittedly limited. We stress the need of using comparative computer simulations – both before and after animal experiments – to better understand animal timing in interaction. We hope this article will serve as a potential first step towards a common computational framework to describe temporal interactions in animals, including humans.

Abstract

The study of human language is progressively moving toward comparative and interactive frameworks, extending the concept of turn‐taking to animal communication. While such an endeavor will help us understand the interactive origins of language, any theoretical account for cross‐species turn‐taking should consider three key points. First, animal turn‐taking must incorporate biological studies on animal chorusing, namely how different species coordinate their signals over time. Second, while concepts employed in human communication and turn‐taking, such as intentionality, are still debated in animal behavior, lower level mechanisms with clear neurobiological bases can explain much of animal interactive behavior. Third, social behavior, interactivity, and cooperation can be orthogonal, and the alternation of animal signals need not be cooperative. Considering turn‐taking a subset of chorusing in the rhythmic dimension may avoid overinterpretation and enhance the comparability of future empirical work.

Abstract

Puppyhood is a very active social and vocal period in a harbor seal's life Phoca vitulina. An important feature of vocalizations is their temporal and rhythmic structure, and understanding vocal timing and rhythms in harbor seals is critical to a cross-species hypothesis in evolutionary neuroscience that links vocal learning, rhythm perception, and synchronization. This study utilized analytical techniques that may best capture rhythmic structure in pup vocalizations with the goal of examining whether (1) harbor seal pups show rhythmic structure in their calls and (2) rhythms evolve over time. Calls of 3 wild-born seal pups were recorded daily over the course of 1-3 weeks; 3 temporal features were analyzed using 3 complementary techniques. We identified temporal and rhythmic structure in pup calls across different time windows. The calls of harbor seal pups exhibit some degree of temporal and rhythmic organization, which evolves over puppyhood and resembles that of other species' interactive communication. We suggest next steps for investigating call structure in harbor seal pups and propose comparative hypotheses to test in other pinniped species.

Abstract

Comparative research investigating how nonhuman animals generalize patterns of auditory stimuli often uses sequences of human speech syllables and reports limited generalization abilities in animals. Here, we reverse this logic, testing humans with stimulus sequences tailored to squirrel monkeys. When test stimuli are familiar (human voices), humans succeed in two types of generalization. However, when the same structural rule is instantiated over unfamiliar but perceivable sounds within squirrel monkeys’ optimal hearing frequency range, human participants master only one type of generalization. These findings have methodological implications for the design of comparative experiments, which should be fair towards all tested species’ proclivities and limitations.

Abstract

Animal communication and motoric behavior develop over time. Often, this temporal dimension has communicative relevance and is organized according to structural patterns. In other words, time is a crucial dimension for rhythm and synchrony in animal movement and communication. Rhythm is defined as temporal structure at a second-millisecond time scale (Kotz et al. 2018). Synchrony is defined as precise co-occurrence of 2 behaviors in time (Ravignani 2017).

Rhythm, synchrony, and other forms of temporal interaction are taking center stage in animal behavior and communication. Several critical questions include, among others: what species show which rhythmic predispositions? How does a species’ sensitivity for, or proclivity towards, rhythm arise? What are the species-specific functions of rhythm and synchrony, and are there functional trends across species? How did similar or different rhythmic behaviors evolved in different species? This Special Column aims at collecting and contrasting research from different species, perceptual modalities, and empirical methods. The focus is on timing, rhythm and synchrony in the second-millisecond range.

Three main approaches are commonly adopted to study animal rhythms, with a focus on: 1) spontaneous individual rhythm production, 2) group rhythms, or 3) synchronization experiments. I concisely introduce them below (see also Kotz et al. 2018; Ravignani et al. 2018).

Abstract

Why does human speech have rhythm? As we cannot travel back in time to witness how speech developed its rhythmic properties and why humans have the cognitive skills to process them, we rely on alternative methods to find out. One powerful tool is the comparative approach: studying the presence or absence of cognitive/behavioral traits in other species to determine which traits are shared between species and which are recent human inventions. Vocalizations of many species exhibit temporal structure, but little is known about how these rhythmic structures evolved, are perceived and produced, their biological and developmental bases, and communicative functions. We review the literature on rhythm in speech and animal vocalizations as a first step toward understanding similarities and differences across species. We extend this review to quantitative techniques that are useful for computing rhythmic structure in acoustic sequences and hence facilitate cross‐species research. We report links between vocal perception and motor coordination and the differentiation of rhythm based on hierarchical temporal structure. While still far from a complete cross‐species perspective of speech rhythm, our review puts some pieces of the puzzle together.

Abstract

Alternative mathematical models predict differences in how animals adjust the timing of their calls. Differences can be measured as the effect of the timing of a conspecific call on the rate and period of calling of a focal animal, and the lag between the two. Here, I test these alternative hypotheses by tapping into harbor seals’ (Phoca vitulina) mechanisms for spontaneous timing. Both socioecology and vocal behavior of harbor seals make them an interesting model species to study call rhythm and timing. Here, a wild-born seal pup was tested in controlled laboratory conditions. Based on previous recordings of her vocalizations and those of others, I designed playback experiments adapted to that specific animal. The call onsets of the animal were measured as a function of tempo, rhythmic regularity, and spectral properties of the playbacks. The pup adapted the timing of her calls in response to conspecifics’ calls. Rather than responding at a fixed time delay, the pup adjusted her calls’ onset to occur at a fraction of the playback tempo, showing a relative-phase antisynchrony. Experimental results were confirmed via computational modeling. This case study lends preliminary support to a classic mathematical model of animal behavior—Hamilton’s selfish herd—in the acoustic domain.

Abstract

Recognizing that two elements within a sequence of variable length depend on each other is a key ability in understanding the structure of language and music. Perception of such interdependencies has previously been documented in chimpanzees in the visual domain and in human infants and common squirrel monkeys with auditory playback experiments, but it remains unclear whether it typifies primates in general. Here, we investigated the ability of common marmosets (Callithrix jacchus) to recognize and respond to such dependencies. We tested subjects in a familiarization-discrimination playback experiment using stimuli composed of pure tones that either conformed or did not conform to a grammatical rule. After familiarization to sequences with dependencies, marmosets spontaneously discriminated between sequences containing and lacking dependencies (‘consistent’ and ‘inconsistent’, respectively), independent of stimulus length. Marmosets looked more often to the sound source when hearing sequences consistent with the familiarization stimuli, as previously found in human infants. Crucially, looks were coded automatically by computer software, avoiding human bias. Our results support the hypothesis that the ability to perceive dependencies at variable distances was already present in the common ancestor of all anthropoid primates (Simiiformes).

Abstract

Strategies used in artificial grammar learning can shed light into the abilities of different species to extract regularities from the environment. In the A(X)nB rule, A and B items are linked, but assigned to different positional categories and separated by distractor items. Open questions are how widespread is the ability to extract positional regularities from A(X)nB patterns, which strategies are used to encode positional regularities and whether individuals exhibit preferences for absolute or relative position encoding. We used visual arrays to investigate whether cotton-top tamarins (Saguinusoedipus) can learn this rule and which strategies they use. After training on a subset of exemplars, two of the tested monkeys successfully generalized to novel combinations. These tamarins discriminated between categories of tokens with different properties (A, B, X) and detected a positional relationship between non-adjacent items even in the presence of novel distractors. The pattern of errors revealed that successful subjects used visual similarity with training stimuli to solve the task and that successful tamarins extracted the relative position of As and Bs rather than their absolute position, similarly to what has been observed in other species. Relative position encoding appears to be favoured in different tasks and taxa. Generalization, though, was incomplete, since we observed a failure with items that during training had always been presented in reinforced arrays, showing the limitations in grasping the underlying positional rule. These results suggest the use of local strategies in the extraction of positional rules in cotton-top tamarins.

Abstract

This editorial serves a number of purposes. First, it aims at summarizing and discussing 33 accepted contributions to the special issue “The evolution of rhythm cognition: Timing in music and speech.” The major focus of the issue is the cognitive neuroscience of rhythm, intended as a neurobehavioral trait undergoing an evolutionary process. Second, this editorial provides the interested reader with a guide to navigate the interdisciplinary contributions to this special issue. For this purpose, we have compiled Table 1, where methods, topics, and study species are summarized and related across contributions. Third, we also briefly highlight research relevant to the evolution of rhythm that has appeared in other journals while this special issue was compiled. Altogether, this editorial constitutes a summary of rhythm research in music and speech spanning two years, from mid-2015 until mid-2017

Abstract

Vocal communication is a crucial aspect of animal behavior. The mechanism which most mammals use to vocalize relies on three anatomical components. First, air overpressure is generated inside the lower vocal tract. Second, as the airstream goes through the glottis, sound is produced via vocal fold vibration. Third, this sound is further filtered by the geometry and length of the upper vocal tract. Evidence from mammalian anatomy and bioacoustics suggests that some of these three components may covary with an animal’s body size. The framework provided by acoustic allometry suggests that, because vocal tract length (VTL) is more strongly constrained by the growth of the body than vocal fold length (VFL), VTL generates more reliable acoustic cues to an animal’s size. This hypothesis is often tested acoustically but rarely anatomically, especially in pinnipeds. Here, we test the anatomical bases of the acoustic allometry hypothesis in harbor seal pups Phoca vitulina. We dissected and measured vocal tract, vocal folds, and other anatomical features of 15 harbor seals post-mortem. We found that, while VTL correlates with body size, VFL does not. This suggests that, while body growth puts anatomical constraints on how vocalizations are filtered by harbor seals’ vocal tract, no such constraints appear to exist on vocal folds, at least during puppyhood. It is particularly interesting to find anatomical constraints on harbor seals’ vocal tracts, the same anatomical region partially enabling pups to produce individually distinctive vocalizations.

Abstract

Research on the evolution of human speech and phonology benefits from the comparative approach: structural, spectral, and temporal features can be extracted and compared across species in an attempt to reconstruct the evolutionary history of human speech. Here we focus on analytical tools to measure and compare temporal structure in human speech and animal vocalizations. We introduce the reader to a range of statistical methods usable, on the one hand, to quantify rhythmic complexity in single vocalizations, and on the other hand, to compare rhythmic structure between multiple vocalizations. These methods include: time series analysis, distributional measures, variability metrics, Fourier transform, auto- and cross-correlation, phase portraits, and circular statistics. Using computer-generated data, we apply a range of techniques, walking the reader through the necessary software and its functions. We describe which techniques are most appropriate to test particular hypotheses on rhythmic structure, and provide possible interpretations of the tests. These techniques can be equally well applied to find rhythmic structure in gesture, movement, and any other behavior developing over time, when the research focus lies on its temporal structure. This introduction to quantitative techniques for rhythm and timing analysis will hopefully spur additional comparative research, and will produce comparable results across all disciplines working on the evolution of speech, ultimately advancing the field.

Abstract

Isochrony is crucial to the rhythm of human music. Some neural, behavioral and anatomical traits underlying rhythm perception and production are shared with a broad range of species. These may either have a common evolutionary origin, or have evolved into similar traits under different evolutionary pressures. Other traits underlying rhythm are rare across species, only found in humans and few other animals. Isochrony, or stable periodicity, is common to most human music, but isochronous behaviors are also found in many species. It appears paradoxical that humans are particularly good at producing and perceiving isochronous patterns, although this ability does not conceivably confer any evolutionary advantage to modern humans. This article will attempt to solve this conundrum. To this end, we define the concept of isochrony from the present functional perspective of physiology, cognitive neuroscience, signal processing, and interactive behavior, and review available evidence on isochrony in the signals of humans and other animals. We then attempt to resolve the paradox of isochrony by expanding an evolutionary hypothesis about the function that isochronous behavior may have had in early hominids. Finally, we propose avenues for empirical research to examine this hypothesis and to understand the evolutionary origin of isochrony in general.

Abstract

STRUCTURE IN MUSICAL RHYTHM CAN BE MEASURED using a number of analytical techniques. While some techniques—like circular statistics or grammar induction—rely on strong top-down assumptions, assumption-free techniques can only provide limited insights on higher-order rhythmic structure. I suggest that research in music perception and performance can benefit from systematically adopting phase space plots, a visualization technique originally developed in mathematical physics that overcomes the aforementioned limitations. By jointly plotting adjacent interonset intervals (IOI), the motivic rhythmic structure of musical phrases, if present, is visualized geometrically without making any a priori assumptions concerning isochrony, beat induction, or metrical hierarchies. I provide visual examples and describe how particular features of rhythmic patterns correspond to geometrical shapes in phase space plots. I argue that research on music perception and systematic musicology stands to benefit from this descriptive tool, particularly in comparative analyses of rhythm production. Phase space plots can be employed as an initial assumption-free diagnostic to find higher order structures (i.e., beyond distributional regularities) before proceeding to more specific, theory-driven analyses.

Abstract

In response to: How to learn about teaching: An evolutionary framework for the study of teaching behavior in humans and other animals

Arguments about the nature of teaching have depended principally on naturalistic observation and some experimental work. Additional measurement tools, and physiological variations and manipulations can provide insights on the intrinsic structure and state of the participants better than verbal descriptions alone: namely, time-series analysis, and examination of the role of hormones and neuromodulators on the behaviors of teacher and pupil.

Abstract

Comparative pattern learning experiments investigate how different species find regularities in sensory input, providing insights into cognitive processing in humans and other animals. Past research has focused either on one species’ ability to process pattern classes or different species’ performance in recognizing the same pattern, with little attention to individual and species-specific heuristics and decision strategies. We trained and tested two bird species, pigeons (Columba livia) and kea (Nestor notabilis, a parrot species), on visual patterns using touch-screen technology. Patterns were composed of several abstract elements and had varying degrees of structural complexity. We developed a model selection paradigm, based on regular expressions, that allowed us to reconstruct the specific decision strategies and cognitive heuristics adopted by a given individual in our task. Individual birds showed considerable differences in the number, type and heterogeneity of heuristic strategies adopted. Birds’ choices also exhibited consistent species-level differences. Kea adopted effective heuristic strategies, based on matching learned bigrams to stimulus edges. Individual pigeons, in contrast, adopted an idiosyncratic mix of strategies that included local transition probabilities and global string similarity. Although performance was above chance and quite high for kea, no individual of either species provided clear evidence of learning exactly the rule used to generate the training stimuli. Our results show that similar behavioral outcomes can be achieved using dramatically different strategies and highlight the dangers of combining multiple individuals in a group analysis. These findings, and our general approach, have implications for the design of future pattern learning experiments, and the interpretation of comparative cognition research more generally.

Abstract

Humans have a strong proclivity for structuring and patterning stimuli: Whether in space or time, we tend to mentally order stimuli in our environment and organize them into units with specific types of relationships. A crucial prerequisite for such organization is the cognitive ability to discern and process regularities among multiple stimuli. To investigate the evolutionary roots of this cognitive capacity, we tested chimpanzees—which, along with bonobos, are our closest living relatives—for simple, variable distance dependency processing in visual patterns. We trained chimpanzees to identify pairs of shapes either linked by an arbitrary learned association (arbitrary associative dependency) or a shared feature (same shape, feature-based dependency), and to recognize strings where items related to either of these ways occupied the first (leftmost) and the last (rightmost) item of the stimulus. We then probed the degree to which subjects generalized this pattern to new colors, shapes, and numbers of interspersed items. We found that chimpanzees can learn and generalize both types of dependency rules, indicating that the ability to encode both feature-based and arbitrary associative regularities over variable distances in the visual domain is not a human prerogative. Our results strongly suggest that these core components of human structural processing were already present in our last common ancestor with chimpanzees.

Abstract

Flexibly adapting social behavior to social and environmental challenges helps to alleviate glucocorticoid (GC) levels, which may have positive fitness implications for an individual. For primates, the predominant social behavior is grooming. Giving grooming to others is particularly efficient in terms of GC mitigation. However, grooming is confined by certain limitations such as time constraints or restricted access to other group members. For instance, dominance hierarchies may impact grooming partner availability in primate societies. Consequently specific grooming patterns emerge. In despotic species focusing grooming activity on preferred social partners significantly ameliorates GC levels in females of all ranks. In this study we investigated grooming patterns and GC management in Barbary macaques, a comparably relaxed species. We monitored changes in grooming behavior and cortisol (C) for females of different ranks. Our results show that the C‐amelioration associated with different grooming patterns had a gradual connection with dominance hierarchy: while higher‐ranking individuals showed lowest urinary C measures when they focused their grooming on selected partners within their social network, lower‐ranking individuals expressed lowest C levels when dispersing their grooming activity evenly across their social partners. We argue that the relatively relaxed social style of Barbary macaque societies allows individuals to flexibly adapt grooming patterns, which is associated with rank‐specific GC management. Am. J. Primatol. 77:688–700, 2015