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.

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.

Damage to the prefrontal cortex increases utilitarian moral judgements.

The psychological and neurobiological processes underlying moral judgement have been the focus of many recent empirical studies. Of central interest is whether emotions play a causal role in moral judgement, and, in parallel, how emotion-related areas of the brain contribute to moral judgement. Here we show that six patients with focal bilateral damage to the ventromedial prefrontal cortex (VMPC), a brain region necessary for the normal generation of emotions and, in particular, social emotions, produce an abnormally 'utilitarian' pattern of judgements on moral dilemmas that pit compelling considerations of aggregate welfare against highly emotionally aversive behaviours (for example, having to sacrifice one person's life to save a number of other lives). In contrast, the VMPC patients' judgements were normal in other classes of moral dilemmas. These findings indicate that, for a selective set of moral dilemmas, the VMPC is critical for normal judgements of right and wrong. The findings support a necessary role for emotion in the generation of those judgements.

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.

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.

Syntax-induced pattern deafness.

Perceptual systems often force systematically biased interpretations upon sensory input. These interpretations are obligatory, inaccessible to conscious control, and prevent observers from perceiving alternative percepts. Here we report a similarly impenetrable phenomenon in the domain of language, where the syntactic system prevents listeners from detecting a simple perceptual pattern. Healthy human adults listened to three-word sequences conforming to patterns readily learned even by honeybees, rats, and sleeping human neonates. Specifically, sequences either started or ended with two words from the same syntactic category (e.g., noun-noun-verb or verb-verb-noun). Although participants readily processed the categories and learned repetition patterns over nonsyntactic categories (e.g., animal-animal-clothes), they failed to learn the repetition pattern over syntactic categories, even when explicitly instructed to look for it. Further experiments revealed that participants successfully learned the repetition patterns only when they were consistent with syntactically possible structures, irrespective of whether these structures were attested in English or in other languages unknown to the participants. When the repetition patterns did not match such syntactically possible structures, participants failed to learn them. Our results suggest that when human adults hear a string of nouns and verbs, their syntactic system obligatorily attempts an interpretation (e.g., in terms of subjects, objects, and predicates). As a result, subjects fail to perceive the simpler pattern of repetitions--a form of syntax-induced pattern deafness that is reminiscent of how other perceptual systems force specific interpretations upon sensory input.

Five-month-old infants' identification of the sources of vocalizations.

Humans speak, monkeys grunt, and ducks quack. How do we come to know which vocalizations animals produce? Here we explore this question by asking whether young infants expect humans, but not other animals, to produce speech, and further, whether infants have similarly restricted expectations about the sources of vocalizations produced by other species. Five-month-old infants matched speech, but not human nonspeech vocalizations, specifically to humans, looking longer at static human faces when human speech was played than when either rhesus monkey or duck calls were played. They also matched monkey calls to monkey faces, looking longer at static rhesus monkey faces when rhesus monkey calls were played than when either human speech or duck calls were played. However, infants failed to match duck vocalizations to duck faces, even though infants likely have more experience with ducks than monkeys. Results show that by 5 months of age, human infants generate expectations about the sources of some vocalizations, mapping human faces to speech and rhesus faces to rhesus calls. Infants' matching capacity does not appear to be based on a simple associative mechanism or restricted to their specific experiences. We discuss these findings in terms of how infants may achieve such competence, as well as its specificity and relevance to acquiring language.

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.

Our chimpanzee mind.

Some might consider the title of this piece preposterous. Bishop Wilberforce would no doubt have shaken his fist at it, just as he disputed Huxley's championing of darwinian continuity. But the title of this essay is no more outrageous than one entitled 'The chimpanzee's bird brain', for there has been extensive evolutionary conservation of many neural and psychological functions across species. We share with chimpanzees some--but not all--mental functions, some of which are shared with other species as well. As the publication of the chimpanzee genome reveals, we also share a good deal of our DNA. Unfortunately, we are virtually in the dark when it comes to understanding how genes build minds. If comparative genomics is to enlighten our understanding of human origins, it must be accompanied by an equally rich description of animal psychology, both in terms of its underlying neural signatures and the evolutionary processes that led to convergence and divergence with other species.

Predation: Prey plumage adaptation against falcon attack.

Several plumage types are found in feral pigeons (Columba livia), but one type imparts a clear survival advantage during attacks by the swiftest of all predators--the peregrine falcon (Falco peregrinus). Here we use quantitative field observations and experiments to demonstrate both the selective nature of the falcon's choice of prey and the effect of plumage coloration on the survival of feral pigeons. This plumage colour is an independently heritable trait that is likely to be an antipredator adaptation against high-speed attacks in open air space.

Evolving the capacity to understand actions, intentions, and goals.

We synthesize the contrasting predictions of motor simulation and teleological theories of action comprehension and present evidence from a series of studies showing that monkeys and apes-like humans-extract the meaning of an event by (a) going beyond the surface appearance of actions, attributing goals and intentions to the agent; (b) using details about the environment to infer when an action is rational or irrational; (c) making predictions about an agent's goal and the most probable action to obtain the goal, within the constraints of the situation; (d) predicting the most probable outcome of actions even when they are physiologically incapable of producing the actions; and (e) combining information about means and outcomes to make decisions about social interactions, some with moral relevance. These studies reveal the limitations of motor simulation theories, especially those that rely on the notion of direct matching and mirror neuron activation. They provide support, however, for a teleological theory, rooted in an inferential process that extracts information about action means, potential goals, and the environmental constraints that limit rational action.

The evolutionary origins of human patience: temporal preferences in chimpanzees, bonobos, and human adults.

To make adaptive choices, individuals must sometimes exhibit patience, forgoing immediate benefits to acquire more valuable future rewards [1-3]. Although humans account for future consequences when making temporal decisions [4], many animal species wait only a few seconds for delayed benefits [5-10]. Current research thus suggests a phylogenetic gap between patient humans and impulsive, present-oriented animals [9, 11], a distinction with implications for our understanding of economic decision making [12] and the origins of human cooperation [13]. On the basis of a series of experimental results, we reject this conclusion. First, bonobos (Pan paniscus) and chimpanzees (Pan troglodytes) exhibit a degree of patience not seen in other animals tested thus far. Second, humans are less willing to wait for food rewards than are chimpanzees. Third, humans are more willing to wait for monetary rewards than for food, and show the highest degree of patience only in response to decisions about money involving low opportunity costs. These findings suggest that core components of the capacity for future-oriented decisions evolved before the human lineage diverged from apes. Moreover, the different levels of patience that humans exhibit might be driven by fundamental differences in the mechanisms representing biological versus abstract rewards.

The role of emotion in moral psychology.

Recent work in the cognitive and neurobiological sciences indicates an important relationship between emotion and moral judgment. Based on this evidence, several researchers have argued that emotions are the source of our intuitive moral judgments. However, despite the richness of the correlational data between emotion and morality, we argue that the current neurological, behavioral, developmental and evolutionary evidence is insufficient to demonstrate that emotion is necessary for making moral judgments. We suggest instead, that the source of moral judgments lies in our causal-intentional psychology; emotion often follows from these judgments, serving a primary role in motivating morally relevant action.

The apes' edge: positional learning in chimpanzees and humans.

A wide variety of organisms produce actions and signals in particular temporal sequences, including the motor actions recruited during tool-mediated foraging, the arrangement of notes in the songs of birds, whales and gibbons, and the patterning of words in human speech. To accurately reproduce such events, the elements that comprise such sequences must be memorized. Both memory and artificial language learning studies have revealed at least two mechanisms for memorizing sequences, one tracking co-occurrence statistics among items in sequences (i.e., transitional probabilities) and the other one tracking the positions of items in sequences, in particular those of items in sequence-edges. The latter mechanism seems to dominate the encoding of sequences after limited exposure, and to be recruited by a wide array of grammatical phenomena. To assess whether humans differ from other species in their reliance on one mechanism over the other after limited exposure, we presented chimpanzees (Pan troglodytes) and human adults with brief exposure to six items, auditory sequences. Each sequence consisted of three distinct sound types (X, A, B), arranged according to two simple temporal rules: the A item always preceded the B item, and the sequence-edges were always occupied by the X item. In line with previous results with human adults, both species primarily encoded positional information from the sequences; that is, they kept track of the items that occurred in the sequence-edges. In contrast, the sensitivity to co-occurrence statistics was much weaker. Our results suggest that a mechanism to spontaneously encode positional information from sequences is present in both chimpanzees and humans and may represent the default in the absence of training and with brief exposure. As many grammatical regularities exhibit properties of this mechanism, it may be recruited by language and constrain the form that certain grammatical regularities take.

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.

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.

Action comprehension in non-human primates: motor simulation or inferential reasoning?

Some argue that action comprehension is intimately connected with the observer's own motor capacities, whereas others argue that action comprehension depends on non-motor inferential mechanisms. We address this debate by reviewing comparative studies that license four conclusions: monkeys and apes extract the meaning of an action (i) by going beyond the surface properties of actions, attributing goals and intentions to the agent; (ii) by using environmental information to infer when actions are rational; (iii) by making predictions about an agent's goal, and the most probable action to obtain the goal given environmental constraints; (iv) in situations in which they are physiologically incapable of producing the actions. Motor theories are, thus, insufficient to account for primate action comprehension in the absence of inferential mechanisms.

Evidence of an evolutionary precursor to human language affixation in a non-human primate.

Human language, and grammatical competence in particular, relies on a set of computational operations that, in its entirety, is not observed in other animals. Such uniqueness leaves open the possibility that components of our linguistic competence are shared with other animals, having evolved for non-linguistic functions. Here, we explore this problem from a comparative perspective, asking whether cotton-top tamarin monkeys (Saguinus oedipus) can spontaneously (no training) acquire an affixation rule that shares important properties with our inflectional morphology (e.g. the rule that adds -ed to create the past tense, as in the transformation of walk into walk-ed). Using playback experiments, we show that tamarins discriminate between bisyllabic items that start with a specific 'prefix' syllable and those that end with the same syllable as a 'suffix'. These results suggest that some of the computational mechanisms subserving affixation in a diversity of languages are shared with other animals, relying on basic perceptual or memory primitives that evolved for non-linguistic functions.