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Faces and voices are the dominant social signals used to recognize individuals amongst human and nonhuman primates 1–5. Yet, evidence that information across these signals can be integrated into a modality-independent representation of individual identity in the primate brain has been reported only in human patients 6–9. Here we show that, like humans, single neurons in the marmoset monkey hippocampus exhibit invariant neural responses when presented with the faces or voices of specific individuals. However, we also identified a population of single neurons in hippocampus that were responsive to the cross-modal identity of multiple conspecifics, not only a single individual. An identity network model revealed population-level, cross-modal representations of individuals in hippocampus, underscoring the broader contributions of many neurons to encode identity. This pattern was further evidenced by manifold projections of population activity which likewise showed separability of individuals, as well as clustering for family members, suggesting that multiple learned social categories are encoded as related dimensions of identity in hippocampus. The constellation of findings presented here reveal a novel perspective on the neural basis of identity representations in primate hippocampus as being both invariant to modality and comprising multiple levels of acquired social knowledge.

Gene therapy offers great promise in addressing neuropathologies associated with the central and peripheral nervous systems (CNS and PNS). However, genetic access remains difficult, reflecting the critical need for the development of effective and non-invasive gene delivery vectors across species. To that end, we evolved adeno-associated virus serotype 9 (AAV9) capsid in mice and validated two capsids, AAV-MaCPNS1 and AAV-MaCPNS2, across rodent species (mice and rats) and non-human primate (NHP) species (marmosets and rhesus macaques). Intravenous administration of either AAV efficiently transduced the PNS in rodents and both the PNS and CNS in NHPs. Furthermore, we used AAV-MaCPNS1 in mice to systemically deliver the following: (1) the neuronal sensor jGCaMP8s to record calcium signal dynamics in nodose ganglia and (2) the neuronal actuator DREADD to dorsal root ganglia to mediate pain. This conclusively demonstrates the translatability of these two systemic AAVs across four species and their functional utility through proof-of-concept studies in mice.

A foundational pressure in the evolution of all animals is the ability to travel through the world, inherently coupling the sensory and motor systems. While this relationship has been explored in several species

Here, we examined prey-capture in wild common marmosets (Callithrix jacchus) to explicate the active role of primate vision for high-precision, goal-directed motor actions in challenging natural environments. We observed distinct marmoset hunting strategies that each relied on the close integration of visual processes and dynamic biomechanical motor movements, but differed based on several factors including prey size/speed, substrate, and their relative distance to the prey. Marmoset positional behavior in these complex arboreal settings often involves extending the body, including inversions, while relying on vision to guide prey capture. Applying markerless pose estimation technology, analyses revealed details of how primate vision both guides and corrects rapid motor actions in real-time during prey-capture in the wild. These findings illustrate the significance of active vision during primate ethological behaviors in response to the very challenges the visual system evolved to solve.

The core functional organization of the primate brain is remarkably conserved across the order, but behavioral differences evident between species likely reflect derived modifications in the underlying neural processes. Here, we performed the first study to directly compare visual recognition memory in two primate species—rhesus macaques and marmoset monkeys—on the same visual preferential looking task as a first step toward identifying similarities and differences in this cognitive process across the primate phylogeny. Preferences in looking behavior on the task were broadly similar between the species, with greater looking times for novel images compared with repeated images as well as a similarly strong preference for faces compared with other categories. Unexpectedly, we found large behavioral differences among the two species in looking behavior independent of image familiarity. Marmosets exhibited longer looking times, with greater variability compared with macaques, regardless of image content or familiarity. Perhaps most strikingly, marmosets shifted their gaze across the images more quickly, suggesting a different behavioral strategy when viewing images. Although such differences limit the comparison of recognition memory across these closely related species, they point to interesting differences in the mechanisms underlying active vision that have significant implications for future neurobiological investigations with these two nonhuman primate species. Elucidating whether these patterns are reflective of species or broader phylogenetic differences (e.g., between New World and Old World monkeys) necessitates a broader sample of primate taxa from across the Order.

BACKGROUND: A survey was developed to characterize disease incidence, common pathology lesions, environmental characteristics, and nutrition programs within captive research marmoset colonies. METHODS: 17 research facilities completed the electronic survey. RESULTS: Nutritional management programs varied amongst research institutions housing marmosets; eight primary base diets were reported. The most common clinical syndromes reported were gastrointestinal (GI) disease (i.e. inflammatory bowel disease (IBD) like disease, chronic lymphocytic enteritis (CLE), chronic malabsorption, chronic diarrhea), metabolic bone disease or fracture, infectious diarrhea, and oral disease (tooth root abscesses, gingivitis, tooth root resorption). The five most common pathology morphologic diagnoses were colitis, nephropathy/ nephritis, enteritis, chronic lymphoplasmacytic enteritis, and cholecystitis. Obesity was more common (average 20% of a reporting institution’s population) than thin body condition (average 5%). CONCLUSIONS: Through review of current practices, we aim to inspire development of evidence based practices to standardize husbandry and nutrition practices for marmoset research colonies.

A fundamental challenge for audition is parsing the voice of a single speaker amid a cacophony of other voices known as the Cocktail Party Problem (CPP). Despite its prevalence, relatively little remains known about how our simian cousins solve the CPP for active, natural communication. Here we employed an innovative, multi-speaker paradigm comprising five computer-generated Virtual Monkeys (VM) whose respective vocal behavior could be systematically varied to construct marmoset cocktail parties and tested the impact of specific acoustic scene manipulations on vocal behavior. Results indicate that marmosets not only employ auditory mechanisms – including attention – for speaker stream segregation, but also selectively change their own vocal behavior in response to the dynamics of the acoustic scene to overcome the challenges of the CPP. These findings suggest notable parallels between human and nonhuman primate audition and highlight the active role that speakers play to optimize communicative efficacy in complex real-world acoustic scenes.

SummaryWe tested whether social signal processing in more traditional, head-restrained contexts is representative of the putative natural analog – social communication – by comparing responses to vocalizations within individual neurons in marmoset prefrontal cortex (PFC) across a series of behavioral contexts ranging from traditional to naturalistic. Although vocalization responsive neurons were evident in all contexts, cross-context consistency was notably limited. A response to these social signals when subjects were head-restrained was not predictive of a comparable neural response to the identical vocalizations during natural communication, even within the same neuron. Neural activity at the population level followed a similar pattern, as PFC activity could be reliably decoded for the context in which vocalizations were heard. This suggests that neural representations of social signals in primate PFC are not static, but highly flexible and likely reflect how nuances of the dynamic behavioral contexts affect the perception of these signals and what they communicate.

Integrated recording of neural electrical potentials from the brain poses great challenges due to stringent dynamic range requirements to resolve small-signal amplitudes buried in noise amidst large artifact and stimulation transients, as well as stringent power and volume constraints to enable minimally invasive untethered operation. Here, we present a 16-channel neural recording system-on-chip with greater than 90-dB input dynamic range and less than 1- $\mu \text{V}_{\mathrm {rms}}$ input-referred noise from dc to 500 Hz, at 0.8- $\mu \text{W}$ power consumption, and 0.024-mm2 area per channel in a 65-nm CMOS process. Each recording channel features a hybrid analog–digital second-order oversampling analog-to-digital converter (ADC), with the biopotential signal coupling directly to the second integrator for high conversion gain and dynamic offset subtraction in the digital domain. This bypasses the need for high-pass filtering pre-amplification in neural recording systems, which often leads to signal distortion. The integrated ADC-direct neural recording offers record figure-of-merit with a noise efficiency factor (NEF) of the combined front end and ADC of 1.81, and a corresponding power efficiency factor (PEF) of 2.6. Predictive digital autoranging of the binary quantizer further supports rapid transient recovery while maintaining fully dc-coupled operation. Hence, the neural ADC is capable of recording ${\le}$ 0.01-Hz slow potentials as well as recovering from $\ge$ 200-mVpp transients within ${\le}$ 1 ms that are important prerequisites to effective electrocortical recording for brain activity mapping. In vivo recordings from marmoset primate frontal cortex demonstrate its unique capabilities in resolving ultra-slow local field potentials indicative of subject arousal state.

The primate auditory cortex is organized into a network of anatomically and functionally distinct processing fields. Because of its tonotopic properties, the auditory core has been the main target of neurophysiological studies ranging from sensory encoding to perceptual decision-making. By comparison, the auditory belt has been less extensively studied, in part due to the fact that neurons in the belt areas prefer more complex stimuli and integrate over a wider frequency range than neurons in the core, which prefer pure tones of a single frequency. Complementary approaches, such as functional magnetic resonance imaging (fMRI), allow the anatomical identification of both the auditory core and belt and facilitate their functional characterization by rapidly testing a range of stimuli across multiple brain areas simultaneously that can be used to guide subsequent neural recordings. Bridging these technologies in primates will serve to further expand our understanding of primate audition. Here, we developed a novel preparation to test whether different areas of the auditory cortex could be identified using fMRI in common marmosets (Callithrix jacchus), a powerful model of the primate auditory system. We used two types of stimulation, band pass noise and pure tones, to parse apart the auditory core from surrounding secondary belt fields. In contrast to most auditory fMRI experiments in primates, we employed a continuous sampling paradigm to rapidly collect data with little deleterious effects. Here we found robust bilateral auditory cortex activation in two marmosets and unilateral activation in a third utilizing this preparation. Furthermore, we confirmed results previously reported in electrophysiology experiments, such as the tonotopic organization of the auditory core and regions activating preferentially to complex over simple stimuli. Overall, these data establish a key preparation for future research to investigate various functional properties of marmoset auditory cortex.

Communication is an inherently interactive process that weaves together the fabric of both human and nonhuman primate societies. To investigate the properties of the primate brain during active social signaling, we recorded the responses of frontal cortex neurons as freely moving marmosets engaged in conversational exchanges with a visually occluded virtual marmoset. We found that small changes in firing rate (∼1 Hz) occurred across a broadly distributed population of frontal cortex neurons when marmosets heard a conspecific vocalization, and that these changes corresponded to subjects' likelihood of producing or withholding a vocal reply. Although the contributions of individual neurons were relatively small, large populations of neurons were able to clearly distinguish between these social contexts. Most significantly, this social context-dependent change in firing rate was evident even before subjects heard the vocalization, indicating that the probability of a conversational exchange was determined by the state of the frontal cortex at the time a vocalization was heard, and not by a decision driven by acoustic characteristics of the vocalization. We found that changes in neural activity scaled with the length of the conversation, with greater changes in firing rate evident for longer conversations. These data reveal specific and important facets of this neural activity that constrain its possible roles in active social signaling, and we hypothesize that the close coupling between frontal cortex activity and this natural, active primate social-signaling behavior facilitates social-monitoring mechanisms critical to conversational exchanges.SIGNIFICANCE STATEMENT We provide evidence for a novel pattern of neural activity in the frontal cortex of freely moving, naturally behaving, marmoset monkeys that may facilitate natural primate conversations. We discovered small (∼1 Hz), but reliable, changes in neural activity that occurred before marmosets even heard a conspecific vocalization that, as a population, almost perfectly predicted whether subjects would produce a vocalization in response. The change in the state of the frontal cortex persisted throughout the conversation and its magnitude scaled linearly with the length of the interaction. We hypothesize that this social context-dependent change in frontal cortex activity is supported by several mechanisms, such as social arousal and attention, and facilitates social monitoring critical for vocal coordination characteristic of human and nonhuman primate conversations.

Vocal learning is a behavioral trait in which the social and acoustic environment shapes the vocal repertoire of individuals. Over the past century, the study of vocal learning has progressed at the intersection of ecology, physiology, neuroscience, molecular biology, genomics, and evolution. Yet, despite the complexity of this trait, vocal learning is frequently described as a binary trait, with species being classified as either vocal learners or vocal non-learners. As a result, studies have largely focused on a handful of species for which strong evidence for vocal learning exists. Recent studies, however, suggest a continuum in vocal learning capacity across taxa. Here, we further suggest that vocal learning is a multi-component behavioral phenotype comprised of distinct yet interconnected modules. Discretizing the vocal learning phenotype into its constituent modules would facilitate integration of findings across a wider diversity of species, taking advantage of the ways in which each excels in a particular module, or in a specific combination of features. Such comparative studies can improve understanding of the mechanisms and evolutionary origins of vocal learning. We propose an initial set of vocal learning modules supported by behavioral and neurobiological data and highlight the need for diversifying the field in order to disentangle the complexity of the vocal learning phenotype.

Neuroscience is enjoying a renaissance of discovery due in large part to the implementation of next-generation molecular technologies. The advent of genetically encoded tools has complemented existing methods and provided researchers the opportunity to examine the nervous system with unprecedented precision and to reveal facets of neural function at multiple scales. The weight of these discoveries, however, has been technique-driven from a small number of species amenable to the most advanced gene-editing technologies. To deepen interpretation and build on these breakthroughs, an understanding of nervous system evolution and diversity are critical. Evolutionary change integrates advantageous variants of features into lineages, but is also constrained by pre-existing organization and function. Ultimately, each species’ neural architecture comprises both properties that are species-specific and those that are retained and shared. Understanding the evolutionary history of a nervous system provides interpretive power when examining relationships between brain structure and function. The exceptional diversity of nervous systems and their unique or unusual features can also be leveraged to advance research by providing opportunities to ask new questions and interpret findings that are not accessible in individual species. As new genetic and molecular technologies are added to the experimental toolkits utilized in diverse taxa, the field is at a key juncture to revisit the significance of evolutionary and comparative approaches for next-generation neuroscience as a foundational framework for understanding fundamental principles of neural function.

There has been recent increasing interest in the use of marmosets, a New World primate species, as a model in biomedical research. One of the principal advantages of marmosets as a research model is their rich vocal repertoire and communicative vocal behaviors displayed both in the wild and in captivity. Studies of this species' vocal communication system have the potential to reveal the evolutionary underpinnings of human speech, and therefore are of interest to the neuroscience and biology research communities. Here a recent research into the behavioral and neurobiological basis of marmoset vocal communication was reviewed and they argued for their broader value as a neuroscientific model. They discuss potential avenues for future research including developmental neurobiology and the application of modern molecular tools to the study of primate communication. © 2016 Wiley Periodicals, Inc. Develop Neurobiol 77: 286-299, 2017.

The common marmoset (Callithrix jacchus) has garnered interest recently as a powerful model for the future of neuroscience research. Much of this excitement has centered on the species’ reproductive biology and compatibility with gene editing techniques, which together have provided a path for transgenic marmosets to contribute to the study of disease as well as basic brain mechanisms. In step with technical advances is the need to establish experimental paradigms that optimally tap into the marmosets’ behavioral and cognitive capacities. While conditioned task performance of a marmoset can compare unfavorably with rhesus monkey performance on conventional testing paradigms, marmosets’ social cognition and communication are more similar to that of humans. For example, marmosets are amongst only a handful of primates that, like humans, routinely pair bond and care cooperatively for their young. They are also notably pro-social and exhibit social cognitive abilities, such as imitation, that are rare outside of the Apes. In this review, we describe key facets of marmoset natural social behavior and demonstrate that emerging behavioral paradigms are well suited to isolate components of marmoset cognition that are highly relevant to humans. These approaches generally embrace natural behavior and communication, which has been rare in conventional primate testing, and thus allow for a new consideration of neural mechanisms underlying primate social cognition and communication. We anticipate that through parallel technical and paradigmatic advances, marmosets will become an essential model of human social behavior, including its dysfunction in nearly all neuropsychiatric disorders.

The hippocampus comprises two neural signals—place cells and θ oscillations—that contribute to facets of spatial navigation. Although their complementary relationship has been well established in rodents, their respective contributions in the primate brain during free navigation remains unclear. Here, we recorded neural activity in the hippocampus of freely moving marmosets as they naturally explored a spatial environment to more explicitly investigate this issue. We report place cells in marmoset hippocampus during free navigation that exhibit remarkable parallels to analogous neurons in other mammalian species. Although θ oscillations were prevalent in the marmoset hippocampus, the patterns of activity were notably different than in other taxa. This local field potential oscillation occurred in short bouts (approximately .4 s)—rather than continuously—and was neither significantly modulated by locomotion nor consistently coupled to place-cell activity. These findings suggest that the relationship between place-cell activity and θ oscillations in primate hippocampus during free navigation differs substantially from rodents and paint an intriguing comparative picture regarding the neural basis of spatial navigation across mammals., A neurophysiology study of marmoset monkey hippocampus during free navigation identified place cells analogous to those seen in other species, but the limited interaction observed between the activity of these neurons and theta oscillations suggests notable divergence from rodent models.

In cooperatively breeding species, encounters with intruders may serve multiple functions ranging from reaffirming group territory ranges to facilitating assessments for additional breeding opportunities. While these distinctive events offer the opportunity to investigate the delicate balance of these social dimensions within animal societies, their unpredictable occurrence makes witnessing and controlling these events in the wild particularly challenging. Here we used a field playback approach to simulate conspecific territorial incursions in cooperatively breeding common marmosets (Callithrix jacchus) to distinguish between the three following non-mutually exclusive functions of intergroup encounters in this species of New World primate: territorial defense, mate defense, and assessment of breeding opportunities. For these experiments, we systematically broadcast species-typical long-distance contact calls – phees – commonly used in intergroup interactions from the core and periphery of the groups’ territories using either male or female vocalizations. Consistent with a territorial defense hypothesis, a group’s reaction was independent of the simulated intruder’s sex and the response strength was greater when the playback stimulus was broadcast from the core areas of groups’ territories relative to stimulus broadcast from periphery areas. However, sex differences in some facets of their responses suggest that this is not the only potential function for these encounters. Mated males and females started to move first in response to simulated intruders of the opposite sex, suggesting that these events offered opportunities to assess extra-pair breeding opportunities, while the occurrence of females’ piloerection towards simulated female intruders is suggestive of mate-guarding. These data provide unique experimental evidence for the theory that excursions by conspecific intruders may serve multiple functions in a cooperatively breeding vertebrate and are reflective of the known complexities of common marmoset sociobiology.

High-density multi-channel neural recording is critical to driving advances in neuroscience and neuroengineering through increasing the spatial resolution and dynamic range of brain-machine interfaces. Neural-signal-acquisition ICs have conventionally been designed composed of two distinct functional blocks per recording channel: a low-noise amplifier front-end (AFE), and an analog-digital converter (ADC) [1,2]. Hybrid architectures utilizing oversampling ADCs with digital feedback [3-5] have seen recent adoption due to their increased power and area efficiency. Still, input dynamic range (DR) is relatively limited due to aggressive supply voltage scaling and/or kT/C sampling noise. This paper presents a neural-recording ADC chip with 92dB input dynamic range and 0.99μV rms of noise at 0.8μW power consumption per channel over 500Hz signal bandwidth, owing to 1) a predictive digital autoranging (PDA) scheme in a hybrid analog-digital 2nd-order oversampling ADC architecture, 2) no specific sampling process through capacitors, avoiding kT/C noise altogether. Digitally predicting the analog input at 12b resolution from a 1b quantization of the continuously integrated residue at effective 32 oversampling ratio (OSR), the PDA handles a ±130mV electrode differential offset (EDO) and recovers from >200mV pp transient artifacts within

Modern spike sorting techniques are heavily reliant on unsupervised machine learning algorithms for isolation of single-unit activity from noisy channel recordings. One of the most common methods, k-means clustering, is highly sensitive to the number of clusters selected (k) prior to analysis. A robust automated method for determining k is required, in particular for the large datasets currently being analyzed by the Neuroscience community. Information criteria, often applied for this analysis, can yield over-fitted clustering recommendations and employ strong assumptions about cluster gaussianity which do not necessarily hold for real in-vivo neuro-electrophysiological recordings. An algorithmic approach to spike sorting is applied utilizing tandem multi-level wavelet decomposition and principal component analysis to construct a discriminant feature space. K-means clustering is applied to this feature space using a variety of distance metrics to determine which approach yields optimal cluster separation. Clustering outcomes are evaluated using the Entropic Product, an information entropy-based measure that makes no assumptions about the underlying distribution of spikes within a cluster. This measure is demonstrated to be more informative about clustering outcomes than other information criteria when sorting spike data collected using bundled microwire arrays implanted in the Primary Visual Cortex of marmosets conducting a visual-stimulation task.

An audience can have a profound effect on the dynamics of communicative interactions. As a result, non-human primates often adjust their social decision-making strategies depending on the audience composition at a given time. Here we sought to test how the unique vocal behaviour of multiple audience members affected decisions to communicate. To address this issue, we developed a novel experimental paradigm in which common marmosets directly interacted with multiple ‘virtual monkeys’ (VMs), each of whom represented an individual marmoset with distinct vocal behaviour. This active social signalling paradigm provided subjects an opportunity to interact with and learn about the behaviour of each VM in the network and apply this knowledge in subsequent communicative decisions. We found that subjects' propensity to interact with particular VMs was determined by the behaviour of each VM in the audience and suggests that marmoset social decision-making strategies are highly adaptive to nuances of the immediate communication network.

Noisy acoustic environments present several challenges for the evolution of acoustic communication systems. Among the most significant is the need to limit degradation of spectro-temporal signal structure in order to maintain communicative efficacy. This can be achieved by selecting for several potentially complementary processes. Selection can act on behavioral mechanisms permitting signalers to control the timing and occurrence of signal production to avoid acoustic interference. Likewise, the signal itself may be the target of selection, biasing the evolution of its structure to comprise acoustic features that avoid interference from ambient noise or degrade minimally in the habitat. Here, we address the latter topic for common marmoset (Callithrix jacchus) long-distance contact vocalizations, known as phee calls. Our aim was to test whether this vocalization is specifically adapted for transmission in a species-typical forest habitat, the Atlantic forests of northeastern Brazil. We combined seasonal analyses of ambient habitat acoustics with experiments in which pure tones, clicks, and vocalizations were broadcast and rerecorded at different distances to characterize signal degradation in the habitat. Ambient sound was analyzed from intervals throughout the day and over rainy and dry seasons, showing temporal regularities across varied timescales. Broadcast experiment results indicated that the tone and click stimuli showed the typically inverse relationship between frequency and signaling efficacy. Although marmoset phee calls degraded over distance with marked predictability compared with artificial sounds, they did not otherwise appear to be specially designed for increased transmission efficacy or minimal interference in this habitat. We discuss these data in the context of other similar studies and evidence of potential behavioral mechanisms for avoiding acoustic interference in order to maintain effective vocal communication in common marmosets.

Optogenetics has revolutionized the study of functional neuronal circuitry (Boyden ES, Zhang F, Bamberg E, Nagel G, Deisseroth K. Nat Neurosci 8: 1263–1268, 2005; Deisseroth K. Nat Methods 8: 26–29, 2011). Although these techniques have been most successfully implemented in rodent models, they have the potential to be similarly impactful in studies of nonhuman primate brains. Common marmosets ( Callithrix jacchus) have recently emerged as a candidate primate model for gene editing, providing a potentially powerful model for studies of neural circuitry and disease in primates. The application of viral transduction methods in marmosets for identifying and manipulating neuronal circuitry is a crucial step in developing this species for neuroscience research. In the present study we developed a novel, chronic method to successfully induce rapid photostimulation in individual cortical neurons transduced by adeno-associated virus to express channelrhodopsin (ChR2) in awake marmosets. We found that large proportions of neurons could be effectively photoactivated following viral transduction and that this procedure could be repeated for several months. These data suggest that techniques for viral transduction and optical manipulation of neuronal populations are suitable for marmosets and can be combined with existing behavioral preparations in the species to elucidate the functional neural circuitry underlying perceptual and cognitive processes.

There has been recent increasing interest in the use of marmosets, a New World primate species, as a model in biomedical research. One of the principal advantages of marmosets as a research model is their rich vocal repertoire and communicative vocal behaviors displayed both in the wild and in captivity. Studies of this species' vocal communication system have the potential to reveal the evolutionary underpinnings of human speech, and therefore are of interest to the neuroscience and biology research communities. Here a recent research into the behavioral and neurobiological basis of marmoset vocal communication was reviewed and they argued for their broader value as a neuroscientific model. They discuss potential avenues for future research including developmental neurobiology and the application of modern molecular tools to the study of primate communication. © 2016 Wiley Periodicals, Inc. Develop Neurobiol 77: 286-299, 2017.

This edited volume on Psychological Mechanisms in Animal Communication highlights research on the sensory, perceptual, and cognitive mechanisms that underlie signaling and receiving. It brings together researchers working on a broad range of conceptual questions in diverse animal systems and using an assortment of empirical tools. Collectively, these researchers seek to understand how signalers signal and receivers receive. This introductory chapter introduces the major questions in studies of signaler and receiver psychology that are explored in greater depth in subsequent chapters. In so doing, this chapter makes the case that a research agenda aimed at elucidating the mechanisms of signaler and receiver psychology complements and enriches several current areas of animal communication research, in particular those focused on signal design and the parallels and precursors of human language in animals. Ultimately, the goal of this volume is to lay a solid foundation for broader and more comparative studies that investigate the psychological mechanisms of animal communication.

In many species, communication is anything but the effortless task it appears. While many animals communicate with apparent ease, there are serious challenges that need to be overcome for effective signal production and reception. Primates, like many species, are faced with communicative barriers in both their ecological and social landscapes. The ecological landscape is often cluttered with biotic and abiotic noise as potential sources of signal masking and degradation , while the social landscape is riddled with the nuances of the complex relationships that exist between individuals. Here, we consider how different facets of these landscapes pose challenges for communication and discuss research examining how common marmosets (Callithrix jacchus) overcome these obstacles. We emphasize the importance of decision-making and behavioral flexibility with regard to if and when vocalizations are produced in order to optimize effective communication. The strategies presented here are likely to exist across other primate species and reflect the broader social cognitive mechanisms within the primate Order.

Twenty years ago, a new conceptual paradigm known as 'receiver psychology' was introduced to explain the evolution of animal communication systems. This paradigm advanced the idea that psychological processes in the receiver's nervous system influence a signal's detectability, discriminability and memorability, and thereby serve as powerful sources of selection shaping signal design. While advancing our understanding of signal diversity, more recent studies make clear that receiver psychology, as a paradigm, has been structured too narrowly and does not incorporate many of the perceptual and cognitive processes of signal reception that operate between sensory transduction and a receiver's response. Consequently, the past two decades of research on receiver psychology have emphasized considerations of signal evolution but failed to ask key questions about the mechanisms of signal reception and their evolution. The primary aim of this essay is to advocate for a broader receiver psychology paradigm that more explicitly includes a research focus on receivers' psychological landscapes. We review recent experimental studies of hearing and sound communication to illustrate how considerations of several general perceptual and cognitive processes will facilitate future research on animal signalling systems. We also emphasize how a rigorous comparative approach to receiver psychology is critical to explicating the full range of perceptual and cognitive processes involved in receiving and responding to signals.

SUMMARY The natural environment is inherently noisy with acoustic interferences. It is, therefore, beneficial for a species to modify its vocal production to effectively communicate in the presence of interfering noises. Non-human primates have been traditionally considered to possess limited voluntary vocal control, but little is known about their ability to modify vocal behavior when encountering interfering noises. Here we tested the ability of the common marmoset (Callithrix jacchus) to control the initiation of vocalizations and maintain vocal interactions between pairs in an acoustic environment in which the length and predictability (periodic or random aperiodic occurrences) of interfering noise bursts were varied. Despite the presence of interfering noise, the marmosets continued to engage in antiphonal calling behavior. Results showed that the overwhelming majority of calls were initiated during silence gaps even when the length of the silence gap following each noise burst was unpredictable. During the periodic noise conditions, as the length of the silence gap decreased, the latency between the end of noise burst and call onset decreased significantly. In contrast, when presented with aperiodic noise bursts, the marmosets chose to call predominantly during long (4 and 8 s) over short (2 s) silence gaps. In the 8 s periodic noise conditions, a marmoset pair either initiated both calls of an antiphonal exchange within the same silence gap or exchanged calls in two consecutive silence gaps. Our findings provide compelling evidence that common marmosets are capable of modifying their vocal production according to the dynamics of their acoustic environment during vocal communication.

Vocalizations are a dominant means of communication for numerous species, including nonhuman primates. These acoustic signals are encoded with a rich array of information available to signal receivers that can be used to guide species-typical behaviors. In this study, we examined the communicative content of common marmoset phee calls, the species-typical long distance contact call, during antiphonal calling. This call type has a relatively stereotyped acoustic structure, consisting of a series of long tonal pulses. Analyses revealed that calls could be reliably classified based on the individual identity and social group of the caller. Our analyses did not, however, correctly classify phee calls recorded under different social contexts, although differences were evident along individual acoustic parameters. Further tests of antiphonal calling interactions showed that spontaneously produced phee calls differ from antiphonal phee calls in their peak and end frequency, which may be functionally significant. Overall, this study shows that the marmoset phee call has a rich communicative content encoded in its acoustic structure available to conspecifics during antiphonal calling exchanges.

The vocal motor plan is one of the most fundamental and poorly understood elements of primate vocal production. Here we tested whether a single vocal motor plan comprises the full length of a vocalization. We hypothesized that if a single motor plan was determined at vocal onset, the acoustic features early in the call should be predictive of the subsequent call structure. Analyses were performed on two classes of features in marmoset phee calls: continuous and discrete. We first generated correlation matrices of all the continuous features of phee calls. Results showed that the start frequency of a phee’s first pulse significantly correlated with all subsequent spectral features. Moreover, significant correlations were evident within the spectral features as well as within the temporal features, but there was little relationship between these measures. Using a discrete feature, ‘the number of pulses in the phee call’, a discriminant function was able to correctly classify the number of pulses in the calls well above chance based solely on the acoustic structure of the call’s first pulse. Together, these data suggest that a vocal motor plan for the complete call structure is established at call onset. These findings provide a key insight into the mechanisms underlying vocal production in nonhuman primates.

Conversational turn-taking is an integral part of language development, as it reflects a confluence of social factors that mitigate communication. Humans coordinate the timing of speech based on the behaviour of another speaker, a behaviour that is learned during infancy. While adults in several primate species engage in vocal turn-taking, the degree to which similar learning processes underlie its development in these non-human species or are unique to language is not clear. We recorded the natural vocal interactions of common marmosets ( Callithrix jacchus ) occurring with both their sibling twins and parents over the first year of life and observed at least two parallels with language development. First, marmoset turn-taking is a learned vocal behaviour. Second, marmoset parents potentially played a direct role in guiding the development of turn-taking by providing feedback to their offspring when errors occurred during vocal interactions similarly to what has been observed in humans. Though species-differences are also evident, these findings suggest that similar learning mechanisms may be implemented in the ontogeny of vocal turn-taking across our Order, a finding that has important implications for our understanding of language evolution.

One of the great strengths of the mouse model is the wide array of genetic tools that have been developed. Striking examples include methods for directed modification of the genome, and for regulated expression or inactivation of genes. Within neuroscience, it is now routine to express reporter genes, neuronal activity indicators, and opsins in specific neuronal types in the mouse. However, there are considerable anatomical, physiological, cognitive, and behavioral differences between the mouse and the human that, in some areas of inquiry, limit the degree to which insights derived from the mouse can be applied to understanding human neurobiology. Several recent advances have now brought into reach the goal of applying these tools to understanding the primate brain. Here we describe these advances, consider their potential to advance our understanding of the human brain and brain disorders, discuss bioethical considerations, and describe what will be needed to move forward., Poitras Center for Affective Disorders Research, Stanley Center for Psychiatric Research, Brain Research Foundation (Science Innovation Award)

Smooth pursuit eye movements stabilize slow-moving objects on the retina by matching eye velocity with target velocity. Two critical components are required to generate smooth pursuit: first, because it is a voluntary eye movement, the subject must select a target to pursue to engage the tracking system; and second, generating smooth pursuit requires a moving stimulus. We examined whether this behavior also exists in the common marmoset, a New World primate that is increasingly attracting attention as a genetic model for mental disease and systems neuroscience. We measured smooth pursuit in two marmosets, previously trained to perform fixation tasks, using the standard Rashbass step-ramp pursuit paradigm. We first measured the aspects of visual motion that drive pursuit eye movements. Smooth eye movements were in the same direction as target motion, indicating that pursuit was driven by target movement rather than by displacement. Both the open-loop acceleration and closed-loop eye velocity exhibited a linear relationship with target velocity for slow-moving targets, but this relationship declined for higher speeds. We next examined whether marmoset pursuit eye movements depend on an active engagement of the pursuit system by measuring smooth eye movements evoked by small perturbations of motion from fixation or during pursuit. Pursuit eye movements were much larger during pursuit than from fixation, indicating that pursuit is actively gated. Several practical advantages of the marmoset brain, including the accessibility of the middle temporal (MT) area and frontal eye fields at the cortical surface, merit its utilization for studying pursuit movements.

The ability to recognize a conspecific signal is essential to communication. In addition to recognizing the type of call, receivers extract a range of information from the signal about the producer, including identity, sex and dialect. Despite the apparent ease with which this is accomplished, few available data address the computational processes underlying recognition. While it is possible that recognition of the signal and its information content occur in a single stage of processing, different components of the signal may be processed separately. Here we present a series of experiments designed to examine this issue in the cottontop tamarin, Saguinus oedipus. Using the tamarins' natural vocal response to hearing their species-specific combination long call (CLC), antiphonal calling, we presented tamarins with manipulated and unmanipulated CLCs and measured both the number of antiphonal responses and the latency to produce an antiphonal call. Results indicated that recognition of the call type and recognition of the caller occur in separate computational stages of signal processing. These data provide insights into how sensory information is organized by a call recognition system.

Within the vocal repertoires of many species, both males and females produce acoustic variants of the same call type. Despite the relative salience of the acoustic features that correlate with the caller's sex, little is known about the functional significance of this acoustic cue. Specifically, do conspecifics use this information when making behavioural decisions, implying that it is meaningful to signal receivers? And, if so, what selective pressures underlie the salience of the sex differences in call structure? Here we present a series of phonotaxis experiments designed to address these issues in the cottontop tamarin, Saguinus oedipus. We focus on the tamarin combination long call (CLC), a species-specific vocalization consisting of one to two chirps followed by three to four whistles, that functions in the context of social isolation and mate attraction. CLCs produced by males had significantly shorter whistles than those produced by females, although there was some overlap in the sex-specific ranges. Sex differences in the acoustic morphology of CLCs elicited consistent selective phonotaxis, suggesting that this acoustic cue is meaningful to signal receivers and that whistle duration is the primary acoustic feature used to determine the sex of the caller. Males preferred female CLCs consisting of the longest whistles, whereas females preferred male CLCs with the shortest whistles, suggesting that sensory biases in tamarins underlie sex differences in CLCs. These preferences persisted even when stimulus calls contained whistle durations that fell outside the natural range.

We examine which acoustic features are relevant for recognition of the cotton-top tamarin (Saguinus oedipus) combination long-call. This vocalization, emitted by both males and females, functions in maintaining group cohesion, territory defense and mate attraction. Using the tamarins' natural antiphonal vocal response to hearing a combination long-call as the primary measure of recognition, we presented subjects with synthetic exemplars of combination long-calls in which we manipulated across one of three acoustic dimensions: frequency, time and amplitude. Results indicated that although acoustic features in the frequency and time domains are important for combination long-call recognition, the changes in amplitude within and between syllables are not. Furthermore, while the fundamental frequency appears to be the used to encode information about the frequency contour, the temporal information is derived from the harmonics. Overall, these results suggest that tamarins use a specific suite of acoustic features for combination long-call recognition.

Few studies have examined whether non-human tool-users understand the properties that are relevant for a tool's function. We tested cotton-top tamarins (Saguinus oedipus) and rhesus macaques (Macaca mulatta) on an expectancy violation procedure designed to assess whether these species make distinctions between the functionally relevant and irrelevant features of a tool. Subjects watched an experimenter use a tool to push a grape down a ramp, and then were presented with different displays in which the features of the original tool (shape, color, orientation) were selectively varied. Results indicated that both species looked longer when a newly shaped stick acted on the grape than when a newly colored stick performed the same action, suggesting that both species perceive shape as a more salient transformation than color. In contrast, tamarins, but not rhesus, attended to changes in the tool's orientation. We propose that some non-human primates begin with a predisposition to attend to a tool's shape and, with sufficient experience, develop a more sophisticated understanding of the features that are functionally relevant to tools.

The common marmoset (Callithrix jacchus), a small-bodied New World primate, offers several advantages to complement vision research in larger primates. Studies in the anesthetized marmoset have detailed the anatomy and physiology of their visual system (Rosa et al., 2009) while studies of auditory and vocal processing have established their utility for awake and behaving neurophysiological investigations (Lu et al., 2001a,b; Eliades and Wang, 2008a,b; Osmanski and Wang, 2011; Remington et al., 2012). However, a critical unknown is whether marmosets can perform visual tasks under head restraint. This has been essential for studies in macaques, enabling both accurate eye tracking and head stabilization for neurophysiology. In one set of experiments we compared the free viewing behavior of head-fixed marmosets to that of macaques, and found that their saccadic behavior is comparable across a number of saccade metrics and that saccades target similar regions of interest including faces. In a second set of experiments we applied behavioral conditioning techniques to determine whether the marmoset could control fixation for liquid reward. Two marmosets could fixate a central point and ignore peripheral flashing stimuli, as needed for receptive field mapping. Both marmosets also performed an orientation discrimination task, exhibiting a saturating psychometric function with reliable performance and shorter reaction times for easier discriminations. These data suggest that the marmoset is a viable model for studies of active vision and its underlying neural mechanisms.

When nonhuman animals vocalize, signal receivers are provided with a range of potential acoustic information concerning the signaler's body size, sex, individual identity, kinship and group membership. Here we explore whether cotton-top tamarins (Saguinus oedipus) extract such information from their species-typical combination long call using a modification of the phonotaxis assay originally designed for studies of anurans and insects. In each trial, we sequentially played long calls produced by two different individuals and then provided test subjects the choice to approach either speaker location. We quantified selective phonotaxis using two different aspects of subjects' behavioural response: the first approach following stimulus presentation and the total number of times subjects approached toward each speaker location. Results from subjects' first approach indicated that tamarins perceived acoustic differences between long calls produced by cagemates, non-cagemate colony members and foreign tamarins. Specifically, males showed a preference to approach foreign females over familiar ones, while females approached cagemate and homeroom males over foreign males. When the total number of approaches made towards each stimulus was analyzed, results revealed that subjects did not selectively approach cagemates over colony members or colony members over foreign tamarins. Subjects did, however, approach cagemates significantly more often than foreign tamarins. Overall, these results suggest that (i) tamarins are able to use acoustic information encoded within a single vocal signal to assess individuality and degree of familiarity, and (ii) the phonotaxis assay, successfully used in research on anuran and insects, is also a powerful tool for studies of nonhuman primate communication.

To investigate the problem of inter- and intraspecific differences on the mirror test, we conducted two experiments on cotton-top tamarins. Experiment 1 employed a technique similar to one used recently on chimpanzees, and provided no evidence of mirror-mediated touching of the marked area. In a control condition, involving colored dye applied to one arm, two subjects also failed to show self-directed touching, even though they clearly looked at their newly dyed arm. Under these test conditions, cotton-top tamarins fail to show mirror-guided self-exploration. Experiment 2 examined whether this failure was due to insufficient mirror exposure, as well as other details of the testing conditions. In particular, we replicated the design of a previously successful experiment on mirror-mediated recognition in tamarins [Hauser et al., 1995], providing four new animals with a protracted period (three weeks) of mirror exposure prior to dying their hair. In parallel with results from Experiment 1, we observed no evidence of mirror-mediated behavior (recognition) in Experiment 2.

Theories about the evolutionary path that led to the neuronal network underlying human language have long generated much heat without light. Using PET imaging, a recent study suggests that monkeys share a circuit for vocal perception with humans, adding some empirical data to the debate.

Noisy acoustic environments present several challenges for the evolution of acoustic communication systems. Among the most significant is the need to limit degradation of spectro-temporal signal structure in order to maintain communicative efficacy. This can be achieved by selecting for several potentially complementary processes. Selection can act on behavioral mechanisms permitting signalers to control the timing and occurrence of signal production to avoid acoustic interference. Likewise, the signal itself may be the target of selection, biasing the evolution of its structure to comprise acoustic features that avoid interference from ambient noise or degrade minimally in the habitat. Here, we address the latter topic for common marmoset (Callithrix jacchus) long-distance contact vocalizations, known as phee calls. Our aim was to test whether this vocalization is specifically adapted for transmission in a species-typical forest habitat, the Atlantic forests of northeastern Brazil. We combined seasonal analyses of ambient habitat acoustics with experiments in which pure tones, clicks, and vocalizations were broadcast and rerecorded at different distances to characterize signal degradation in the habitat. Ambient sound was analyzed from intervals throughout the day and over rainy and dry seasons, showing temporal regularities across varied timescales. Broadcast experiment results indicated that the tone and click stimuli showed the typically inverse relationship between frequency and signaling efficacy. Although marmoset phee calls degraded over distance with marked predictability compared with artificial sounds, they did not otherwise appear to be specially designed for increased transmission efficacy or minimal interference in this habitat. We discuss these data in the context of other similar studies and evidence of potential behavioral mechanisms for avoiding acoustic interference in order to maintain effective vocal communication in common marmosets.

Many vocalizations are encoded with a diversity of acoustic information about the signal producer. Amongst this information content are social categories related to the identity of the caller that are important for determining if and how a signal receiver may interact with that individual. Here, we employed a novel playback method in common marmosets (Callithrix jacchus) to test individual recognition during bouts of antiphonal calling. These experiments utilized custom, interactive playback software that effectively engaged subjects in antiphonal calling using vocalizations produced by a single individual and presented 'probe' vocalization stimuli representing a different individual at specific points within bouts of calling. The aim here was to test whether marmosets would recognize that the probe stimulus was a phee call produced by a different individual. Data indicated that marmosets were able to detect the change in caller identity; subjects produced significantly fewer antiphonal call responses to probe than control stimuli and, in some conditions, exhibited a shorter latency to produce the vocal response. These data suggest that marmosets recognize the identity of the individual during bouts of antiphonal calling. Furthermore, these results provide a methodological foundation for implementing the probe playback procedure to examine a broader range of social categorization during vocal interactions.

All nonhuman primates communicate with conspecifics using vocalizations, a system involving both the production and perception of species-specific vocal signals. Much of the work on the neural basis of primate vocal communication in cortex has focused on the sensory processing of vocalizations, while relatively little data are available for vocal production. Earlier physiological studies in squirrel monkeys had shed doubts on the involvement of primate cortex in vocal behaviors. The aim of the present study was to identify areas of common marmoset (Callithrix jacchus) cortex that are potentially involved in vocal communication. In this study, we quantified cFos expression in three areas of marmoset cortex – frontal, temporal (auditory) and medial temporal – under various vocal conditions. Specifically, we examined cFos expression in these cortical areas during the sensory, motor (vocal production) and sensory-motor components of vocal communication. Our results showed an increase in cFos expression in ventrolateral prefrontal cortex as well as the medial and lateral belt areas of auditory cortex in the vocal perception condition. In contrast, subjects in the vocal production condition resulted in increased cFos expression only in dorsal premotor cortex. During the sensory-motor condition (antiphonal calling), subjects exhibited cFos expression in each of the above areas, as well as increased expression in perirhinal cortex. Overall, these results suggest that various cortical areas outside primary auditory cortex are involved in primate vocal communication. These findings pave the way for further physiological studies of the neural basis of primate vocal communication.