Vocalization Induced CFos Expression in Marmoset Cortex

All non-human 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

Flexible auditory training, psychophysics, and enrichment of common marmosets with an automated, touchscreen-based system

Devising new and more efficient protocols to analyze the phenotypes of non-human primates, as well as their complex nervous systems, is rapidly becoming of paramount importance. This is because with genome-editing techniques, recently adopted to non-human primates, new animal models for fundamental and translational research have been established. One aspect in particular, namely cognitive hearing, has been difficult to assess compared to visual cognition. To address this, we devised autonomous, standardized, and unsupervised training and testing of auditory capabilities of common marmosets with a cage-based standalone, wireless system. All marmosets tested voluntarily operated the device on a daily basis and went from naïve to experienced at their own pace and with ease. Through a series of experiments, here we show, that animals autonomously learn to associate sounds with images; to flexibly discriminate sounds, and to detect sounds of varying loudness. The developed platform and training principles combine in-cage training of common marmosets for cognitive and psychoacoustic assessment with an enriched environment that does not rely on dietary restriction or social separation, in compliance with the 3Rs principle

Physical mechanisms may be as important as brain mechanisms in evolution of speech [Commentary on Ackerman, Hage, & Ziegler. Brain Mechanisms of acoustic communication in humans and nonhuman primates: an evolutionary perspective]

We present two arguments why physical adaptations for vocalization may be as important as neural adaptations. First, fine control over vocalization is not easy for physical reasons, and modern humans may be exceptional. Second, we present an example of a gorilla that shows rudimentary voluntary control over vocalization, indicating that some neural control is already shared with great apes

Brain mechanisms of acoustic communication in humans and nonhuman primates: An evolutionary perspective

Any account of “what is special about the human brain” (Passingham 2008) must specify the neural basis of our unique ability to produce speech and delineate how these remarkable motor capabilities could have emerged in our hominin ancestors. Clinical data suggest that the basal ganglia provide a platform for the integration of primate-general mechanisms of acoustic communication with the faculty of articulate speech in humans. Furthermore, neurobiological and paleoanthropological data point at a two-stage model of the phylogenetic evolution of this crucial prerequisite of spoken language: (i) monosynaptic refinement of the projections of motor cortex to the brainstem nuclei that steer laryngeal muscles, presumably, as part of a “phylogenetic trend” associated with increasing brain size during hominin evolution; (ii) subsequent vocal-laryngeal elaboration of cortico-basal ganglia circuitries, driven by human-specific FOXP2 mutations.;>This concept implies vocal continuity of spoken language evolution at the motor level, elucidating the deep entrenchment of articulate speech into a “nonverbal matrix” (Ingold 1994), which is not accounted for by gestural-origin theories. Moreover, it provides a solution to the question for the adaptive value of the “first word” (Bickerton 2009) since even the earliest and most simple verbal utterances must have increased the versatility of vocal displays afforded by the preceding elaboration of monosynaptic corticobulbar tracts, giving rise to enhanced social cooperation and prestige. At the ontogenetic level, the proposed model assumes age-dependent interactions between the basal ganglia and their cortical targets, similar to vocal learning in some songbirds. In this view, the emergence of articulate speech builds on the “renaissance” of an ancient organizational principle and, hence, may represent an example of “evolutionary tinkering” (Jacob 1977)

Training in a Laboratory Environment: Methods, Effectiveness and Welfare Implications for Two Species of Primate

The use of Positive Reinforcement Training (PRT) for co-operation during routine husbandry and laboratory procedures is widely advocated as a means of promoting the welfare of nonhuman primates. However, while research originating in US zoos provide qualitative descriptions of how PRT may be used in the training of a wide variety of species, quantitative data and evidence to support the view that PRT reduces stress predominately comes from laboratory studies of primates whose training may have used other methods. Despite official guidelines, training is rarely carried out in the UK and the educational and wider organisational structures concerning training, present in the US are largely absent. The techniques used in the UK were assessed through detailed observations recorded when four stump-tailed macaques were trained to co-operate during venipuncture. Data recorded during training sessions showed that although food rewards were given, their delivery was slow and inconsistent. A certain amount of coercion was used which violates a principle of PRT which states that co-operation should be voluntary. The macaques showed increasing resistance to the process and a mild but detrimental effect on the subsequent behaviour of the study animals. When training resumed 18 months later there were considerable improvements in the techniques used. The macaques showed a greater willingness to participate and there were no significant changes in their behaviour when training days were compared to those when training did not take place. The behaviour of the macaques during venipuncture was judged to be arising from engineered compliance rather than voluntary co-operation. However, it was concluded that the technique observed, if carried out correctly, was a reasonable compromise between forced restraint and voluntary co-operation given the paucity of evidence showing the effectiveness of PRT for invasive procedures. However, it was also concluded that the use of coercion should be recognised and provide a focus for future refinement. The effectiveness and welfare implications ofPRT was assessed through the training of common marmosets to target and allow in-homecage weighing and to provide urine samples. It was found that the trained animals perfonned reliably and that time invested in training could be recouped through faster data collection. Following a period of training or increased positive contact with humans, observations of marmoset behaviour showed a decrease in stress related behaviours and an increase in allogrooming supporting the view that improved relations with humans had a beneficial effect. Following exposure to a mild stressor, trained marmosets showed no elevation in levels of urinary cortisol or stress related behaviours. Untrained animals showed increased levels of locomoting and selfscratching following exposure to the same stressor. It was concluded that PRT successfully reduced the stress associated with the presence of, and manipulation by, humans. Final recommendations were that training can promote the welfare of nonhuman primates and should be used in UK laboratories to a greater extent than is currently the case. However, the lack of educational opportunities for animal trainers in the UK needs to be addressed. It was also recommended that in light of the growing evidence showing the benefits that can arise from training and good relations with humans, the zero-handling policy practiced in many UK zoos should be reassessed

Social learning in mixed-species troops of Saguinus fuscicollis and Saguinus labiatus: tests of foraging benefit hypotheses in captivity

The selective costs and benefits affecting the evolution of group living have long interested behavioural ecologists because knowledge of these selective forces can enhance our understanding not only of why organisms live in groups, but also why species exhibit particular patterns of social organisation. Tamarins form stable and permanent mixed-species troops providing an excellent model for examining the costs and benefits hypothesised for group living. However, testing hypotheses in the wild is difficult, not least because participating species are rarely found out of association. In contrast, in captivity it is possible to compare matched single- and mixed-species troops and also to study the same individuals in single and mixed-species troops to see what effect the presence of a congener has on behaviour. In this way, captive work can help us confirm, reject, or refine the hypotheses, and aids in the generation of new ones, for relating back to the wild. The utility of this approach is demonstrated in this thesis which explored some of the foraging benefit hypotheses and, in particular, the underlying notion that individuals in tamarind mixed-species troops can increase their foraging efficiency through social earning. Single and mixed-species troops of Saguinus fuscicollis and S. labiatus were studied at Belfast Zoological Gardens. It was found that social interaction with conspecifics and congeners facilitated learning by individuals of various types of food-related information (food palatability, location, and method of access). However, although social learning operated in mixed-species troops, it did so under the shadow of inter-specific dominance. The results were used, in conjunction with field observations in Bolivia, to make inferences about the adaptive function of social learning in the wild. These findings strengthen the hypotheses which suggest that increased opportunity for social learning, through an increase in troop size and as a result of species divergence in behaviour, is an adaptive advantage of mixed-species troop formation in tamarins

Social Contagion in Common Marmosets (Callithrix jacchus): Implications for Cognition, Culture and Welfare

The social transmission of social behaviours in nonhuman primates has been understudied, experimentally, relative to instrumental, food-related behaviours. This is disproportional in relation to the comparatively high percentage of potential social traditions reported in wild primates. I report a systematic survey of the social learning literature and provide quantitative evidence of the discrepancy (Watson and Caldwell, 2009). Addressing the identified deficit in experimental work on social behaviours, I also report three empirical studies investigating the contagious nature of affective states in captive, socially housed marmosets. I carried out an observational study, to determine whether marmosets are influenced by spontaneously produced neighbour calls to perform a range of behaviours associated with similar affect. My results supported a neighbour effect for anxiety in marmosets. Consistent with previous findings for chimpanzees (Baker and Aureli, 1996; Videan et al., 2005), I also found evidence for neighbour effects for aggression and affiliation (Watson and Caldwell, 2010). Through experimental playback, I investigated contingent social contagion in the auditory and visual modalities. The playback of pre-recorded affiliative (chirp) calls was found to be associated with marmosets spending increased time in a range of affiliative behaviours. Playback of video showing conspecifics engaged in a positive affiliative behaviour (allogrooming) also appeared to cause marmosets to spend longer performing various affiliative behaviours. My results indicate that social contagion of affiliation is a multi-modal phenomenon in marmosets and also represent the first evidence that allogrooming is visually contagious in primates. Sapolsky (2006) conceptualised culture as the performance of species-typical behaviours to an unusual extent, termed ‘social culture’. Researchers have yet to directly investigate a transmission mechanism. I investigated whether a social culture of increased affiliation could be initiated in marmosets through the long-term playback, of positive calls, or of video of positive behaviour. The results were consistent with a relatively long-lasting influence of the playback of affiliative calls across several affiliative behaviours. The effect appeared to last substantially beyond the specific hours of playback, between playbacks, and after playback had ceased, potentially indicating a temporary shift in social culture. These results are preliminary but provide some support for the proposal that auditory social contagion may be a transmission mechanism for social culture. The long-term video playback of allogrooming appeared to result in a transitory shift in performance of the identical behaviour (increased allogrooming) after playbacks had ceased. In addition to theoretical implications for social cognition and social culture, my findings have potential practical application for the enhancement of welfare in captive marmosets through sensory, and non-contact social, enrichment.

Electrophysiological studies of the production and cortical representation of vocalisations in the guinea pig

Vocal production: Guinea pigs (GP) are gregarious animals with a well-characterised repertoire of 11 vocalisations. These are context dependent, communicating information about danger, identity and emotional state. Vocalisations have previously been produced by electrical stimulation of three areas in the GP brain: anterior cingulate, hypothalamus and periaqueductal grey. These vocalisations were reported as natural-sounding, but with little or no spectral analysis to support this assertion. I elicited calls from urethane-anaesthetised GP by stimulating all the above areas, and from the amygdala and several thalamic nuclei. The spectrotemporal properties of these vocalisations were analysed and eight distinct vocal patterns were identified. For comparison, recordings of spontaneous calls from the same colony (Grimsley et al., 2012) were analysed in the same way, then used to name the electrically elicited calls. For six call types the matches between electrically elicited and spontaneous calls were unambiguous. The remaining two elicited calls were identified as being slightly unnatural versions of one spontaneous call. Five calls were produced during the (1.6 s) electrical stimulation and three were produced after the stimulation, lasting up to 30 s. Concurrent bilateral stimulation of loci producing post-stimulus calls always had an additive effect, whereas stimulation of two loci giving during-stimulus calls was more complex. Auditory representation of vocalisations: To date, eight functional areas of GP auditory cortex have been identified using electrophysiology, and their responses to vocalisations has been investigated previously. I have discovered a new area, ventral to those currently described, which was named deep ventrorostral belt (dVRB). It is unresponsive to a broad range of puretone auditory stimuli, yet is highly selective to conspecific vocalisations. Single neuron recordings were taken from dVRB and the primary auditory region (AI) during the audio-vocal study. Audio-vocal interactions: The vocal production system communicates the expected sensory consequences of its action. This allows the auditory system to discriminate between self-produced and external sounds. These sensorimotor connections originate in premotor areas of the midbrain as well as motor planning areas of neo- and paleocortex. The basal amygdala (BA) – an emotion-mediating structure – yields vocalisations in GP when stimulated, and is involved in the affective prosody of human speech. It was hypothesised, therefore, that BA would also have an audio-vocal role. A protocol was developed to combine electrical stimulation in BA with auditory presentation of a range of GP vocalisations, whilst recording neural activity in AI and dVRB. In both cortical areas, single-neuron responses demonstrated a complex interaction of electrical and auditory stimuli; showing both enhanced or suppressed responses, depending on call type