The domestication of the larynx: The neural crest connection.

Wolves howl and dogs bark, both are able to produce variants of either vocalization, but we see a distinct difference in usage between wild and domesticate. Other domesticates also show distinct changes to their vocal output: domestic cats retain meows, a distinctly subadult trait in wildcats. Such differences in acoustic output are well-known, but the causal mechanisms remain little-studied. Potential links between domestication and vocal output are intriguing for multiple reasons, and offer a unique opportunity to explore a prominent hypothesis in domestication research: the neural crest/domestication syndrome hypothesis. This hypothesis suggests that in the early stages of domestication, selection for tame individuals decreased neural crest cell (NCCs) proliferation and migration, which led to a downregulation of the sympathetic arousal system, and hence reduced fear and reactive aggression. NCCs are a transitory stem cell population crucial during embryonic development that tie to diverse tissue types and organ systems. One of these neural-crest derived systems is the larynx, the main vocal source in mammals. We argue that this connection between NCCs and the larynx provides a powerful test of the predictions of the neural crest/domestication syndrome hypothesis, discriminating its predictions from those of other current hypotheses concerning domestication.

Evolutionary novelties underlie sound production in baleen whales.

Baleen whales (mysticetes) use vocalizations to mediate their complex social and reproductive behaviours in vast, opaque marine environments1. Adapting to an obligate aquatic lifestyle demanded fundamental physiological changes to efficiently produce sound, including laryngeal specializations2-4. Whereas toothed whales (odontocetes) evolved a nasal vocal organ5, mysticetes have been thought to use the larynx for sound production1,6-8. However, there has been no direct demonstration that the mysticete larynx can phonate, or if it does, how it produces the great diversity of mysticete sounds9. Here we combine experiments on the excised larynx of three mysticete species with detailed anatomy and computational models to show that mysticetes evolved unique laryngeal structures for sound production. These structures allow some of the largest animals that ever lived to efficiently produce frequency-modulated, low-frequency calls. Furthermore, we show that this phonation mechanism is likely to be ancestral to all mysticetes and shares its fundamental physical basis with most terrestrial mammals, including humans10, birds11, and their closest relatives, odontocetes5. However, these laryngeal structures set insurmountable physiological limits to the frequency range and depth of their vocalizations, preventing them from escaping anthropogenic vessel noise12,13 and communicating at great depths14, thereby greatly reducing their active communication range.

Cellular computation and cognition.

Contemporary neural network models often overlook a central biological fact about neural processing: that single neurons are themselves complex, semi-autonomous computing systems. Both the information processing and information storage abilities of actual biological neurons vastly exceed the simple weighted sum of synaptic inputs computed by the "units" in standard neural network models. Neurons are eukaryotic cells that store information not only in synapses, but also in their dendritic structure and connectivity, as well as genetic "marking" in the epigenome of each individual cell. Each neuron computes a complex nonlinear function of its inputs, roughly equivalent in processing capacity to an entire 1990s-era neural network model. Furthermore, individual cells provide the biological interface between gene expression, ongoing neural processing, and stored long-term memory traces. Neurons in all organisms have these properties, which are thus relevant to all of neuroscience and cognitive biology. Single-cell computation may also play a particular role in explaining some unusual features of human cognition. The recognition of the centrality of cellular computation to "natural computation" in brains, and of the constraints it imposes upon brain evolution, thus has important implications for the evolution of cognition, and how we study it.

Domestic cat larynges can produce purring frequencies without neural input.

Most mammals produce vocal sounds according to the myoelastic-aerodynamic (MEAD) principle, through self-sustaining oscillation of laryngeal tissues.1,2 In contrast, cats have long been believed to produce their low-frequency purr vocalizations through a radically different mechanism involving active muscle contractions (AMC), where neurally driven electromyographic burst patterns (typically at 20-30 Hz) cause the intrinsic laryngeal muscles to actively modulate the respiratory airflow. Direct empirical evidence for this AMC mechanism is sparse.3 Here, the fundamental frequency (fo) ranges of eight domestic cats (Felis silvestris catus) were investigated in an excised larynx setup, to test the prediction of the AMC hypothesis that vibration should be impossible without neuromuscular activity, and thus unattainable in excised larynx setups, which are based on MEAD principles. Surprisingly, all eight excised larynges produced self-sustained oscillations at typical cat purring rates. Histological analysis of cat larynges revealed the presence of connective tissue masses, up to 4 mm in diameter, embedded in the vocal fold.4 This vocal fold specialization appears to allow the unusually low fo values observed in purring. While our data do not fully reject the AMC hypothesis for purring, they show that cat larynges can easily produce sounds in the purr regime with fundamental frequencies of 25 to 30 Hz without neural input or muscular contraction. This strongly suggests that the physical and physiological basis of cat purring involves the same MEAD-based mechanisms as other cat vocalizations (e.g., meows) and most other vertebrate vocalizations but is potentially augmented by AMC.

Hoover the talking seal.

Diandra Duengen and colleagues introduce Hoover, a male harbor seal famous for his imitation of human speech.

Social dynamics impact scolding behaviour in captive groups of common ravens (Corvus corax).

BACKGROUND: Predator avoidance can have immense impacts on fitness, yet individual variation in the expression of anti-predator behaviour remains largely unexplained. Existing research investigating learning of novel predators has focused either on individuals or groups, but not both. Testing in individual settings allows evaluations of learning or personality differences, while testing in group settings makes it impossible to distinguish any such individual differences from social dynamics. In this study, we investigate the effect of social dynamics on individual anti-predator behaviour. We trained 15 captive ravens to recognize and respond to a novel experimental predator and then exposed them to this predator in both group and isolation settings across 1.5 years to tease apart individual differences from social effects and evaluate two hypotheses: (1) weaker anti-predator responses of some individuals in the group occurred, because they failed to recognize the experimental predator as a threat, leading to weak responses when separated, or (2) some individuals had learned the new threat, but their scolding intensity was repressed in the group trials due to social dynamics (such as dominance rank), leading to increased scolding intensity when alone. RESULTS: We found that dominance significantly influences scolding behaviour in the group trials; top-ranked individuals scold more and earlier than lower ranking ones. However, in the separation trials scolding duration is no longer affected by rank. CONCLUSIONS: We speculate that, while top-ranked individuals use their anti-predator responses to signal status in the group, lower-ranking ravens may be suppressed from, or are less capable of, performing intense anti-predator behaviour while in the group. This suggests that, in addition to its recruitment or predator-deterrent effects, alarm calling may serve as a marker of individual quality to conspecifics.

Melodic Intonation Therapy for aphasia: A multi-level meta-analysis of randomized controlled trials and individual participant data.

Melodic Intonation Therapy (MIT) is a prominent rehabilitation program for individuals with post-stroke aphasia. Our meta-analysis investigated the efficacy of MIT while considering quality of outcomes, experimental design, influence of spontaneous recovery, MIT protocol variant, and level of generalization. Extensive literature search identified 606 studies in major databases and trial registers; of those, 22 studies-overall 129 participants-met all eligibility criteria. Multi-level mixed- and random-effects models served to separately meta-analyze randomized controlled trial (RCT) and non-RCT data. RCT evidence on validated outcomes revealed a small-to-moderate standardized effect in noncommunicative language expression for MIT-with substantial uncertainty. Unvalidated outcomes attenuated MIT's effect size compared to validated tests. MIT's effect size was 5.7 times larger for non-RCT data compared to RCT data (g̅case report = 2.01 vs. g̅RCT = 0.35 for validated Non-Communicative Language Expression measures). Effect size for non-RCT data decreased with number of months post-stroke, suggesting confound through spontaneous recovery. Deviation from the original MIT protocol did not systematically alter benefit from treatment. Progress on validated tests arose mainly from gains in repetition tasks rather than other domains of verbal expression, such as everyday communication ability. Our results confirm the promising role of MIT in improving trained and untrained performance on unvalidated outcomes, alongside validated repetition tasks, and highlight possible limitations in promoting everyday communication ability.

The expensive-tissue hypothesis may help explain brain-size reduction during domestication.

Morphological traits, such as white patches, floppy ears and curly tails, are ubiquitous in domestic animals and are referred to as the 'domestication syndrome'. A commonly discussed hypothesis that has the potential to provide a unifying explanation for these traits is the 'neural crest/domestication syndrome hypothesis'. Although this hypothesis has the potential to explain most traits of the domestication syndrome, it only has an indirect connection to the reduction of brain size, which is a typical trait of domestic animals. We discuss how the expensive-tissue hypothesis might help explain brain-size reduction in domestication.

Evolutionary loss of complexity in human vocal anatomy as an adaptation for speech.

Human speech production obeys the same acoustic principles as vocal production in other animals but has distinctive features: A stable vocal source is filtered by rapidly changing formant frequencies. To understand speech evolution, we examined a wide range of primates, combining observations of phonation with mathematical modeling. We found that source stability relies upon simplifications in laryngeal anatomy, specifically the loss of air sacs and vocal membranes. We conclude that the evolutionary loss of vocal membranes allows human speech to mostly avoid the spontaneous nonlinear phenomena and acoustic chaos common in other primate vocalizations. This loss allows our larynx to produce stable, harmonic-rich phonation, ideally highlighting formant changes that convey most phonetic information. Paradoxically, the increased complexity of human spoken language thus followed simplification of our laryngeal anatomy.

Seven-month-old infants detect symmetrical structures in multi-featured abstract visual patterns.

The present study investigated 7-month-old infants' ability to perceive structural symmetry in mosaic-like abstract visual patterns. We examined infants' (n = 98) spontaneous looking behaviour to mosaic-like sequences with symmetrical and asymmetrical structures. Sequences were composed of square tiles from two categories that differed in their colour scheme and internal shape. We manipulated sequence length (3 or 5 tiles) and abstractness of the symmetry (token vs. category level). The 7-month-olds discriminated structurally symmetrical from asymmetrical mosaics in the first half of the test phase (first 8 trials). Sequence length, level of symmetry, or number of unique tiles per sequence did not significantly modulate infants' looking behaviour. These results suggest that very young infants detect differences in structural symmetry in multi-featured visual patterns.

Understanding Design Features of Music and Language: The Choric/Dialogic Distinction.

Music and spoken language share certain characteristics: both consist of sequences of acoustic elements that are combinatorically combined, and these elements partition the same continuous acoustic dimensions (frequency, formant space and duration). However, the resulting categories differ sharply: scale tones and note durations of small integer ratios appear in music, while speech uses phonemes, lexical tone, and non-isochronous durations. Why did music and language diverge into the two systems we have today, differing in these specific features? We propose a framework based on information theory and a reverse-engineering perspective, suggesting that design features of music and language are a response to their differential deployment along three different continuous dimensions. These include the familiar propositional-aesthetic ('goal') and repetitive-novel ('novelty') dimensions, and a dialogic-choric ('interactivity') dimension that is our focus here. Specifically, we hypothesize that music exhibits specializations enhancing coherent production by several individuals concurrently-the 'choric' context. In contrast, language is specialized for exchange in tightly coordinated turn-taking-'dialogic' contexts. We examine the evidence for our framework, both from humans and non-human animals, and conclude that many proposed design features of music and language follow naturally from their use in distinct dialogic and choric communicative contexts. Furthermore, the hybrid nature of intermediate systems like poetry, chant, or solo lament follows from their deployment in the less typical interactive context.

Why evolve consciousness? Neural credit and blame allocation as a core function of consciousness.

I concur with Merker and colleague's critiques, suggesting that hypotheses about the evolutionary function of consciousness can help address them. Brains are parallel systems that function to compute possible actions and predict outcomes. I hypothesize that a core function of consciousness per se is the global feedback of information about those actions actually executed, supporting local learning via neuronal updating.

Cultural evolution: Conserved patterns of melodic evolution across musical cultures.

A new study finds that melodies evolve in similar ways, reminiscent of genetic evolution, across cultures. Patterns of change in music and other aesthetic domains may be the key to understanding how culture evolves when unfettered by physical or ecological constraints.

Cranial volume and palate length of cats, Felis spp., under domestication, hybridization and in wild populations.

Reduced brain size, compared with wild individuals, is argued to be a key characteristic of domesticated mammal species, and often cited as a key component of a putative 'domestication syndrome'. However, brain size comparisons are often based on old, inaccessible literature and in some cases drew comparisons between domestic animals and wild species that are no longer thought to represent the true progenitor species of the domestic species in question. Here we replicate studies on cranial volumes in domestic cats that were published in the 1960s and 1970s, comparing wildcats, domestic cats and their hybrids. Our data indicate that domestic cats indeed, have smaller cranial volumes (implying smaller brains) relative to both European wildcats (Felis silvestris) and the wild ancestors of domestic cats, the African wildcats (Felis lybica), verifying older results. We further found that hybrids of domestic cats and European wildcats have cranial volumes that cluster between those of the two parent species. Apart from replicating these studies, we also present new data on palate length in Felis cat skulls, showing that domestic cat palates are shorter than those of European wildcats but longer than those of African wildcats. Our data are relevant to current discussions of the causes and consequences of the 'domestication syndrome' in domesticated mammals.

Performance of Deaf Participants in an Abstract Visual Grammar Learning Task at Multiple Formal Levels: Evaluating the Auditory Scaffolding Hypothesis.

Previous research has hypothesized that human sequential processing may be dependent upon hearing experience (the "auditory scaffolding hypothesis"), predicting that sequential rule learning abilities should be hindered by congenital deafness. To test this hypothesis, we compared deaf signer and hearing individuals' ability to acquire rules of different computational complexity in a visual artificial grammar learning task using sequential stimuli. As a group, deaf participants succeeded at all levels of the task; Bayesian analysis indicates that they successfully acquired each of several target grammars at ascending levels of the formal language hierarchy. Overall, these results do not support the auditory scaffolding hypothesis. However, age- and education-matched hearing participants did outperform deaf participants in two out of three tested grammars. We suggest that this difference may be related to verbal recoding strategies in the two groups. Any verbal recoding strategies used by the deaf signers would be less effective because they would have to use the same visual channel required for the experimental task.

Vocal flexibility in a eusocial rodent.

Vocal production learning-the ability to learn new sounds-is fundamental to human communication and is also seen in many nonhuman species, including birds, bats, elephants, and marine mammals. A new paper in Science may add an unusual rodent species-the naked mole rat-to this list.

Voice modulatory cues to structure across languages and species.

Voice modulatory cues such as variations in fundamental frequency, duration and pauses are key factors for structuring vocal signals in human speech and vocal communication in other tetrapods. Voice modulation physiology is highly similar in humans and other tetrapods due to shared ancestry and shared functional pressures for efficient communication. This has led to similarly structured vocalizations across humans and other tetrapods. Nonetheless, in their details, structural characteristics may vary across species and languages. Because data concerning voice modulation in non-human tetrapod vocal production and especially perception are relatively scarce compared to human vocal production and perception, this review focuses on voice modulatory cues used for speech segmentation across human languages, highlighting comparative data where available. Cues that are used similarly across many languages may help indicate which cues may result from physiological or basic cognitive constraints, and which cues may be employed more flexibly and are shaped by cultural evolution. This suggests promising candidates for future investigation of cues to structure in non-human tetrapod vocalizations. This article is part of the theme issue 'Voice modulation: from origin and mechanism to social impact (Part I)'.

Information and the single cell.

Understanding the evolution of cognition requires an understanding of the costs and benefits of neural computation. This requires analysis of neuronal circuitry in terms of information-processing efficiency, ultimately cashed out in terms of ATP expenditures relative to adaptive problem-solving abilities. Despite a preoccupation in neuroscience with the synapse as the source of stored neural information, it is clear that, along with synaptic weights and electrochemical dynamics, neurons have multiple mechanisms which store and process information, including 'wetware' (protein phosphorylation, gene transcription, and so on) and cell morphology (dendritic form). Insights into non-synaptic information-processing can be gained by examining the surprisingly complex abilities of single-celled organisms ('cellular cognition') because neurons share many of the same abilities. Cells provide the fundamental level at which information processing interfaces with gene expression, and cell-internal information-processing mechanisms are both powerful and energetically efficient. Understanding cellular computation should be a central goal of research on cognitive evolution.