Cory T. Miller

Amodal completion of acoustic signals by a nonhuman primate

Evidence of amodal completion exists for both visual and auditory stimuli in humans. The importance of this mechanism in forming stable representations of sensory information suggests that it may be common among multiple modalities and species. Here we show that a species of nonhuman primate amodally completes biologically meaningful acoustic stimuli, which provides evidence that the neural mechanism mediating this aspect of auditory perception is shared among primates, and perhaps other taxonomic groups as well.

Sensory-motor interactions modulate a primate vocal behavior: antiphonal calling in common marmosets

A fundamental issue in neuroscience pertains to how different cortical systems interact to generate behavior. One of the most direct ways to address this issue is to investigate how sensory information is encoded and used to produce a motor response. Antiphonal calling is a natural vocal behavior that involves individuals producing their species-specific long distance vocalization in response to hearing the same call and engages both the auditory and motor systems, as well as the cognitive neural systems involved in decision making and categorization. Here we present results from a series of behavioral experiments investigating the auditory–vocal interactions during antiphonal calling in the common marmoset (Callithrix jacchus). We manipulated sensory input by placing subjects in different social contexts and found that the auditory input had a significant effect on call timing and propensity to call. Playback experiments tested the significance of the timing of vocal production in antiphonal calling and showed that a short latency between antiphonal calls was necessary to maintain reciprocal vocal interactions. Overall, this study shows that sensory-motor interactions can be experimentally induced and manipulated in a natural primate vocal behavior. Antiphonal calling represents a promising model system to examine these issues in non-human primates at both the behavioral and neural levels.

Active Vision in Marmosets: A Model System for Visual Neuroscience

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.

Representing tools: how two non-human primate species distinguish between the functionally relevant and irrelevant features of a tool

Few studies have examined whether non-human tool-users understand the properties that are relevant for a tools 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 tools orientation. We propose that some non-human primates begin with a predisposition to attend to a tools shape and, with sufficient experience, develop a more sophisticated understanding of the features that are functionally relevant to tools.

Vocal control by the common marmoset in the presence of interfering noise

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.

The communicative content of the common marmoset phee call during antiphonal calling

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. Am. J. Primatol. 72:974–980, 2010.

Vocal turn-taking in a non-human primate is learned during ontogeny

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.

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.

Cotton-top tamarins (Saguinus oedipus) fail to show mirror-guided self-exploration.

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. Am. J. Primatol. 53:131–137, 2001.

Individual recognition during bouts of antiphonal calling 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.