Macaque claustrum, pulvinar and putative dorsolateral amygdala support the cross-modal association of social audio-visual stimuli based on meaning.

Social communication draws on several cognitive functions such as perception, emotion recognition and attention. The association of audio-visual information is essential to the processing of species-specific communication signals. In this study, we use functional magnetic resonance imaging in order to identify the subcortical areas involved in the cross-modal association of visual and auditory information based on their common social meaning. We identified three subcortical regions involved in audio-visual processing of species-specific communicative signals: the dorsolateral amygdala, the claustrum and the pulvinar. These regions responded to visual, auditory congruent and audio-visual stimulations. However, none of them was significantly activated when the auditory stimuli were semantically incongruent with the visual context, thus showing an influence of visual context on auditory processing. For example, positive vocalization (coos) activated the three subcortical regions when presented in the context of positive facial expression (lipsmacks) but not when presented in the context of negative facial expression (aggressive faces). In addition, the medial pulvinar and the amygdala presented multisensory integration such that audiovisual stimuli resulted in activations that were significantly higher than those observed for the highest unimodal response. Last, the pulvinar responded in a task-dependent manner, along a specific spatial sensory gradient. We propose that the dorsolateral amygdala, the claustrum and the pulvinar belong to a multisensory network that modulates the perception of visual socioemotional information and vocalizations as a function of the relevance of the stimuli in the social context. SIGNIFICANCE STATEMENT: Understanding and correctly associating socioemotional information across sensory modalities, such that happy faces predict laughter and escape scenes predict screams, is essential when living in complex social groups. With the use of functional magnetic imaging in the awake macaque, we identify three subcortical structures-dorsolateral amygdala, claustrum and pulvinar-that only respond to auditory information that matches the ongoing visual socioemotional context, such as hearing positively valenced coo calls and seeing positively valenced mutual grooming monkeys. We additionally describe task-dependent activations in the pulvinar, organizing along a specific spatial sensory gradient, supporting its role as a network regulator.

Socially meaningful visual context either enhances or inhibits vocalisation processing in the macaque brain.

Social interactions rely on the interpretation of semantic and emotional information, often from multiple sensory modalities. Nonhuman primates send and receive auditory and visual communicative signals. However, the neural mechanisms underlying the association of visual and auditory information based on their common social meaning are unknown. Using heart rate estimates and functional neuroimaging, we show that in the lateral and superior temporal sulcus of the macaque monkey, neural responses are enhanced in response to species-specific vocalisations paired with a matching visual context, or when vocalisations follow, in time, visual information, but inhibited when vocalisation are incongruent with the visual context. For example, responses to affiliative vocalisations are enhanced when paired with affiliative contexts but inhibited when paired with aggressive or escape contexts. Overall, we propose that the identified neural network represents social meaning irrespective of sensory modality.

Automated video-based heart rate tracking for the anesthetized and behaving monkey.

Heart rate (HR) is extremely valuable in the study of complex behaviours and their physiological correlates in non-human primates. However, collecting this information is often challenging, involving either invasive implants or tedious behavioural training. In the present study, we implement a Eulerian video magnification (EVM) heart tracking method in the macaque monkey combined with wavelet transform. This is based on a measure of image to image fluctuations in skin reflectance due to changes in blood influx. We show a strong temporal coherence and amplitude match between EVM-based heart tracking and ground truth ECG, from both color (RGB) and infrared (IR) videos, in anesthetized macaques, to a level comparable to what can be achieved in humans. We further show that this method allows to identify consistent HR changes following the presentation of conspecific emotional voices or faces. EVM is used to extract HR in humans but has never been applied to non-human primates. Video photoplethysmography allows to extract awake macaques HR from RGB videos. In contrast, our method allows to extract awake macaques HR from both RGB and IR videos and is particularly resilient to the head motion that can be observed in awake behaving monkeys. Overall, we believe that this method can be generalized as a tool to track HR of the awake behaving monkey, for ethological, behavioural, neuroscience or welfare purposes.

Of mice and men, nature and nurture, and a few red herrings.

Burkart et al.'s proposal is based on three false premises: (1) theories of the mind are either domain-specific/modular (DSM) or domain-general (DG); (2) DSM systems are considered inflexible, built by nature; and (3) animal minds are deemed as purely DSM. Clearing up these conceptual confusions is a necessary first step in understanding how general intelligence evolved.

Sociocultural Influences on Moral Judgments: East-West, Male-Female, and Young-Old.

Gender, age, and culturally specific beliefs are often considered relevant to observed variation in social interactions. At present, however, the scientific literature is mixed with respect to the significance of these factors in guiding moral judgments. In this study, we explore the role of each of these factors in moral judgment by presenting the results of a web-based study of Eastern (i.e., Russia) and Western (i.e., USA, UK, Canada) subjects, male and female, and young and old. Participants (n = 659) responded to hypothetical moral scenarios describing situations where sacrificing one life resulted in saving five others. Though men and women from both types of cultures judged (1) harms caused by action as less permissible than harms caused by omission, (2) means-based harms as less permissible than side-effects, and (3) harms caused by contact as less permissible than by non-contact, men in both cultures delivered more utilitarian judgments (save the five, sacrifice one) than women. Moreover, men from Western cultures were more utilitarian than Russian men, with no differences observed for women. In both cultures, older participants delivered less utilitarian judgments than younger participants. These results suggest that certain core principles may mediate moral judgments across different societies, implying some degree of universality, while also allowing a limited range of variation due to sociocultural factors.

The mystery of language evolution.

Understanding the evolution of language requires evidence regarding origins and processes that led to change. In the last 40 years, there has been an explosion of research on this problem as well as a sense that considerable progress has been made. We argue instead that the richness of ideas is accompanied by a poverty of evidence, with essentially no explanation of how and why our linguistic computations and representations evolved. We show that, to date, (1) studies of nonhuman animals provide virtually no relevant parallels to human linguistic communication, and none to the underlying biological capacity; (2) the fossil and archaeological evidence does not inform our understanding of the computations and representations of our earliest ancestors, leaving details of origins and selective pressure unresolved; (3) our understanding of the genetics of language is so impoverished that there is little hope of connecting genes to linguistic processes any time soon; (4) all modeling attempts have made unfounded assumptions, and have provided no empirical tests, thus leaving any insights into language's origins unverifiable. Based on the current state of evidence, we submit that the most fundamental questions about the origins and evolution of our linguistic capacity remain as mysterious as ever, with considerable uncertainty about the discovery of either relevant or conclusive evidence that can adjudicate among the many open hypotheses. We conclude by presenting some suggestions about possible paths forward.

Conceptual and empirical problems with game theoretic approaches to language evolution.

The importance of game theoretic models to evolutionary theory has been in formulating elegant equations that specify the strategies to be played and the conditions to be satisfied for particular traits to evolve. These models, in conjunction with experimental tests of their predictions, have successfully described and explained the costs and benefits of varying strategies and the dynamics for establishing equilibria in a number of evolutionary scenarios, including especially cooperation, mating, and aggression. Over the past decade or so, game theory has been applied to model the evolution of language. In contrast to the aforementioned scenarios, however, we argue that these models are problematic due to conceptual confusions and empirical difficiences. In particular, these models conflate the comptutations and representations of our language faculty (mechanism) with its utility in communication (function); model languages as having different fitness functions for which there is no evidence; depend on assumptions for the starting state of the system, thereby begging the question of how these systems evolved; and to date, have generated no empirical studies at all. Game theoretic models of language evolution have therefore failed to advance how or why language evolved, or why it has the particular representations and computations that it does. We conclude with some brief suggestions for how this situation might be ameliorated, enabling this important theoretical tool to make substantive empirical contributions.

On recursion.

It is a truism that conceptual understanding of a hypothesis is required for its empirical investigation. However, the concept of recursion as articulated in the context of linguistic analysis has been perennially confused. Nowhere has this been more evident than in attempts to critique and extend Hauseretal's. (2002) articulation. These authors put forward the hypothesis that what is uniquely human and unique to the faculty of language-the faculty of language in the narrow sense (FLN)-is a recursive system that generates and maps syntactic objects to conceptual-intentional and sensory-motor systems. This thesis was based on the standard mathematical definition of recursion as understood by Gödel and Turing, and yet has commonly been interpreted in other ways, most notably and incorrectly as a thesis about the capacity for syntactic embedding. As we explain, the recursiveness of a function is defined independent of such output, whether infinite or finite, embedded or unembedded-existent or non-existent. And to the extent that embedding is a sufficient, though not necessary, diagnostic of recursion, it has not been established that the apparent restriction on embedding in some languages is of any theoretical import. Misunderstanding of these facts has generated research that is often irrelevant to the FLN thesis as well as to other theories of language competence that focus on its generative power of expression. This essay is an attempt to bring conceptual clarity to such discussions as well as to future empirical investigations by explaining three criterial properties of recursion: computability (i.e., rules in intension rather than lists in extension); definition by induction (i.e., rules strongly generative of structure); and mathematical induction (i.e., rules for the principled-and potentially unbounded-expansion of strongly generated structure). By these necessary and sufficient criteria, the grammars of all natural languages are recursive.

Innovative coconut-opening in a semi free-ranging rhesus monkey (Macaca mulatta): A case report on behavioral propensities.

The present case report provides a description of the emergence of an innovative, highly beneficial for- aging behavior in a single rhesus monkey (Macaca mulatta) on the island of Cayo Santiago, Puerto Rico. Selectively choosing the island's cement dock and nearby surrounding rocky terrain, our focal subject (ID: 84 J) opens coconuts using two types of underhand tosses: (1) a rolling motion to move it, and (2) a throwing motion up in the air to crack the shell. We discuss this innovative behavior in light of species-specific behavioral propensities.

What experimental experience affects dogs' comprehension of human communicative actions?

Studies of dogs report that individuals reliably respond to the goal-directed communicative actions (e.g., pointing) of human experimenters. All of these studies use some version of a multi-trial approach, thereby allowing for the possibility of rapid learning within an experimental session. The experiments reported here ask whether dogs can respond correctly to a communicative action based on only a single presentation, thereby eliminating the possibility of learning within the experimental context. We tested 173 dogs. For each dog reaching our test criteria, we used a single presentation of six different goal-directed actions within a session, asking whether they correctly follow to a target goal (container with concealed food) a (1) distal hand point, (2) step toward one container, (3) hand point to one container followed by step toward the other, (4) step toward one container and point to the other, (5) distal foot point with the experimenter's hands free, and (6) distal foot point with the experimenter's hands occupied. Given only a single presentation, dogs selected the correct container when the experimenter hand pointed, foot pointed with hands occupied, or stepped closer to the target container, but failed on the other actions, despite using the same method. The fact that dogs correctly followed foot pointing with hands occupied, but not hands free, suggests that they are sensitive to environmental constraints, and use this information to infer rational, goal-directed action. We discuss these results in light of the role of experience in recognizing communicative gestures, as well as the significance of coding criteria for studies of canine competence.

The influence of type and token frequency on the acquisition of affixation patterns: implications for language processing.

Rules, and exceptions to such rules, are ubiquitous in many domains, including language. Here we used simple artificial grammars to investigate the influence of 2 factors on the acquisition of rules and their exceptions, namely type frequency (the relative numbers of different exceptions to different regular items) and token frequency (the number of exception tokens relative to the number of regular tokens). We familiarized participants to either a prefixation pattern (where regulars started with /ZaI/ and exceptions ended with /ZaI/) or a suffixation pattern (where regulars ended with /ZaI/ and exceptions started with /ZaI/). We show that the type and the token frequency of regular items and exceptions influence in different ways what participants can learn. For the exceptions to be learned, they have to occur sufficiently often so that participants can memorize them; this can be achieved by a high token frequency. However, a high token frequency of the exceptions also impaired the acquisition of the regular pattern. In contrast, the type frequency of the patterns seemed to determine whether the regular pattern could be learned: When the type frequency of the regular items was sufficiently high, participants successfully learned the regular pattern even when the exceptions were played so often that 66% of the familiarization items were exceptions. We discuss these findings in the context of general learning mechanisms and the role they may play in language acquisition.

Serotonin selectively influences moral judgment and behavior through effects on harm aversion.

Aversive emotional reactions to real or imagined social harms infuse moral judgment and motivate prosocial behavior. Here, we show that the neurotransmitter serotonin directly alters both moral judgment and behavior through increasing subjects' aversion to personally harming others. We enhanced serotonin in healthy volunteers with citalopram (a selective serotonin reuptake inhibitor) and contrasted its effects with both a pharmacological control treatment and a placebo on tests of moral judgment and behavior. We measured the drugs' effects on moral judgment in a set of moral 'dilemmas' pitting utilitarian outcomes (e.g., saving five lives) against highly aversive harmful actions (e.g., killing an innocent person). Enhancing serotonin made subjects more likely to judge harmful actions as forbidden, but only in cases where harms were emotionally salient. This harm-avoidant bias after citalopram was also evident in behavior during the ultimatum game, in which subjects decide to accept or reject fair or unfair monetary offers from another player. Rejecting unfair offers enforces a fairness norm but also harms the other player financially. Enhancing serotonin made subjects less likely to reject unfair offers. Furthermore, the prosocial effects of citalopram varied as a function of trait empathy. Individuals high in trait empathy showed stronger effects of citalopram on moral judgment and behavior than individuals low in trait empathy. Together, these findings provide unique evidence that serotonin could promote prosocial behavior by enhancing harm aversion, a prosocial sentiment that directly affects both moral judgment and moral behavior.

Word segmentation with universal prosodic cues.

When listening to speech from one's native language, words seem to be well separated from one another, like beads on a string. When listening to a foreign language, in contrast, words seem almost impossible to extract, as if there was only one bead on the same string. This contrast reveals that there are language-specific cues to segmentation. The puzzle, however, is that infants must be endowed with a language-independent mechanism for segmentation, as they ultimately solve the segmentation problem for any native language. Here, we approach the acquisition problem by asking whether there are language-independent cues to segmentation that might be available to even adult learners who have already acquired a native language. We show that adult learners recognize words in connected speech when only prosodic cues to word-boundaries are given from languages unfamiliar to the participants. In both artificial and natural speech, adult English speakers, with no prior exposure to the test languages, readily recognized words in natural languages with critically different prosodic patterns, including French, Turkish and Hungarian. We suggest that, even though languages differ in their sound structures, they carry universal prosodic characteristics. Further, these language-invariant prosodic cues provide a universally accessible mechanism for finding words in connected speech. These cues may enable infants to start acquiring words in any language even before they are fine-tuned to the sound structure of their native language.

The tuning of human neonates' preference for speech.

Human neonates prefer listening to speech compared to many nonspeech sounds, suggesting that humans are born with a bias for speech. However, neonates' preference may derive from properties of speech that are not unique but instead are shared with the vocalizations of other species. To test this, thirty neonates and sixteen 3-month-olds were presented with nonsense speech and rhesus monkey vocalizations. Neonates showed no preference for speech over rhesus vocalizations but showed a preference for both these sounds over synthetic sounds. In contrast, 3-month-olds preferred speech to rhesus vocalizations. Neonates' initial biases minimally include speech and monkey vocalizations. These listening preferences are sharpened over 3 months, yielding a species-specific preference for speech, paralleling findings on infant face perception.

Disruption of the right temporoparietal junction with transcranial magnetic stimulation reduces the role of beliefs in moral judgments.

When we judge an action as morally right or wrong, we rely on our capacity to infer the actor's mental states (e.g., beliefs, intentions). Here, we test the hypothesis that the right temporoparietal junction (RTPJ), an area involved in mental state reasoning, is necessary for making moral judgments. In two experiments, we used transcranial magnetic stimulation (TMS) to disrupt neural activity in the RTPJ transiently before moral judgment (experiment 1, offline stimulation) and during moral judgment (experiment 2, online stimulation). In both experiments, TMS to the RTPJ led participants to rely less on the actor's mental states. A particularly striking effect occurred for attempted harms (e.g., actors who intended but failed to do harm): Relative to TMS to a control site, TMS to the RTPJ caused participants to judge attempted harms as less morally forbidden and more morally permissible. Thus, interfering with activity in the RTPJ disrupts the capacity to use mental states in moral judgment, especially in the case of attempted harms.

Damage to ventromedial prefrontal cortex impairs judgment of harmful intent.

Moral judgments, whether delivered in ordinary experience or in the courtroom, depend on our ability to infer intentions. We forgive unintentional or accidental harms and condemn failed attempts to harm. Prior work demonstrates that patients with damage to the ventromedial prefrontal cortex (VMPC) deliver abnormal judgments in response to moral dilemmas and that these patients are especially impaired in triggering emotional responses to inferred or abstract events (e.g., intentions), as opposed to real or actual outcomes. We therefore predicted that VMPC patients would deliver abnormal moral judgments of harmful intentions in the absence of harmful outcomes, as in failed attempts to harm. This prediction was confirmed in the current study: VMPC patients judged attempted harms, including attempted murder, as more morally permissible relative to controls. These results highlight the critical role of the VMPC in processing harmful intent for moral judgment.

The origins of religion: evolved adaptation or by-product?

Considerable debate has surrounded the question of the origins and evolution of religion. One proposal views religion as an adaptation for cooperation, whereas an alternative proposal views religion as a by-product of evolved, non-religious, cognitive functions. We critically evaluate each approach, explore the link between religion and morality in particular, and argue that recent empirical work in moral psychology provides stronger support for the by-product approach. Specifically, despite differences in religious background, individuals show no difference in the pattern of their moral judgments for unfamiliar moral scenarios. These findings suggest that religion evolved from pre-existing cognitive functions, but that it may then have been subject to selection, creating an adaptively designed system for solving the problem of cooperation.