Perceptual specializations for processing species-specific vocalizations in the common marmoset (Callithrix jacchus).

How humans and animals segregate sensory information into discrete, behaviorally meaningful categories is one of the hallmark questions in neuroscience. Much of the research around this topic in the auditory system has centered around human speech perception, in which categorical processes result in an enhanced sensitivity for acoustically meaningful differences and a reduced sensitivity for nonmeaningful distinctions. Much less is known about whether nonhuman primates process their species-specific vocalizations in a similar manner. We address this question in the common marmoset, a small arboreal New World primate with a rich vocal repertoire produced across a range of behavioral contexts. We first show that marmosets perceptually categorize their vocalizations in ways that correspond to previously defined call types for this species. Next, we show that marmosets are differentially sensitive to changes in particular acoustic features of their most common call types and that these sensitivity differences are matched to the population statistics of their vocalizations in ways that likely maximize category formation. Finally, we show that marmosets are less sensitive to changes in these acoustic features when within the natural range of variability of their calls, which possibly reflects perceptual specializations which maintain existing call categories. These findings suggest specializations for categorical vocal perception in a New World primate species and pave the way for future studies examining their underlying neural mechanisms.

Constraints on vocal production learning in budgerigars (Melopsittacus undulates).

Budgerigars (Melopsittacus undulatus) are small Australian parrots with a well-documented, learned vocal repertoire and a high degree of vocal production learning. These birds live in large, social flocks and they vocally interact with each other in a dynamic, reciprocal manner. We assume that budgerigars must process and integrate a wide variety of sensory stimuli when selecting appropriate vocal responses to conspecifics during vocal interactions, but the relative contributions of these different stimuli to that process are next to impossible to tease apart in a natural context. Here we show that budgerigars, under operant control, can learn to respond to specific stimuli with a specific vocal response. Budgerigars were trained to produce contact calls to a combination of auditory and visual cues. Birds learned to produce specific contact calls to stimuli that differed either in location (visual or auditory) or quality (visual). Interestingly, the birds could not learn to associate different vocal responses with different auditory stimuli coming from the same location. Surprisingly, this was so even when the auditory stimuli and the responses were the same (i.e., the bird's own contact call). These results show that even in a highly controlled operant context, acoustic cues alone were not sufficient to support vocal production learning in budgerigars. From a different perspective, these results highlight the significant role that social interaction likely plays in vocal production learning so elegantly shown by Irene Pepperberg's work in parrots.

Complex pitch perception mechanisms are shared by humans and a New World monkey.

The perception of the pitch of harmonic complex sounds is a crucial function of human audition, especially in music and speech processing. Whether the underlying mechanisms of pitch perception are unique to humans, however, is unknown. Based on estimates of frequency resolution at the level of the auditory periphery, psychoacoustic studies in humans have revealed several primary features of central pitch mechanisms. It has been shown that (i) pitch strength of a harmonic tone is dominated by resolved harmonics; (ii) pitch of resolved harmonics is sensitive to the quality of spectral harmonicity; and (iii) pitch of unresolved harmonics is sensitive to the salience of temporal envelope cues. Here we show, for a standard musical tuning fundamental frequency of 440 Hz, that the common marmoset (Callithrix jacchus), a New World monkey with a hearing range similar to that of humans, exhibits all of the primary features of central pitch mechanisms demonstrated in humans. Thus, marmosets and humans may share similar pitch perception mechanisms, suggesting that these mechanisms may have emerged early in primate evolution.

Behavioral dependence of auditory cortical responses.

Neural responses in the auditory cortex have historically been measured from either anesthetized or awake but non-behaving animals. A growing body of work has begun to focus instead on recording from auditory cortex of animals actively engaged in behavior tasks. These studies have shown that auditory cortical responses are dependent upon the behavioral state of the animal. The longer ascending subcortical pathway of the auditory system and unique characteristics of auditory processing suggest that such dependencies may have a more profound influence on cortical processing in the auditory system compared to other sensory systems. It is important to understand the nature of these dependencies and their functional implications. In this article, we review the literature on this topic pertaining to cortical processing of sounds.

A quantitative acoustic analysis of the vocal repertoire of the common marmoset (Callithrix jacchus).

The common marmoset (Callithrix jacchus), a highly vocal New World primate species, has emerged in recent years as a promising animal model for studying brain mechanisms underlying perception, vocal production, and cognition. The present study provides a quantitative acoustic analysis of a large number of vocalizations produced by marmosets in a social environment within a captive colony. Previous classifications of the marmoset vocal repertoire were mostly based on qualitative observations. In the present study a variety of vocalizations from individually identified marmosets were sampled and multiple acoustic features of each type of vocalization were measured. Results show that marmosets have a complex vocal repertoire in captivity that consists of multiple vocalization types, including both simple calls and compound calls composed of sequences of simple calls. A detailed quantification of the vocal repertoire of the marmoset can serve as a solid basis for studying the behavioral significance of their vocalizations and is essential for carrying out studies that investigate such properties as perceptual boundaries between call types and among individual callers as well as neural coding mechanisms for vocalizations. It can also serve as the basis for evaluating abnormal vocal behaviors resulting from diseases or genetic manipulations.

The role of harmonic resolvability in pitch perception in a vocal nonhuman primate, the common marmoset (Callithrix jacchus).

Pitch is one of the most fundamental percepts in the auditory system and can be extracted using either spectral or temporal information in an acoustic signal. Although pitch perception has been extensively studied in human subjects, it is far less clear how nonhuman primates perceive pitch. We have addressed this question in a series of behavioral studies in which marmosets, a vocal nonhuman primate species, were trained to discriminate complex harmonic tones differing in either spectral (fundamental frequency [f0]) or temporal envelope (repetition rate) cues. We found that marmosets used temporal envelope information to discriminate pitch for acoustic stimuli with higher-order harmonics and lower f0 values and spectral information for acoustic stimuli with lower-order harmonics and higher f0 values. We further measured frequency resolution in marmosets using a psychophysical task in which pure tone thresholds were measured as a function of notched noise masker bandwidth. Results show that only the first four harmonics are resolved at low f0 values and up to 16 harmonics are resolved at higher f0 values. Resolvability in marmosets is different from that in humans, where the first five to nine harmonics are consistently resolved across most f0 values, and is likely the result of a smaller marmoset cochlea. In sum, these results show that marmosets use two mechanisms to extract pitch (harmonic templates [spectral] for resolved harmonics, and envelope extraction [temporal] for unresolved harmonics) and that species differences in stimulus resolvability need to be taken into account when investigating and comparing mechanisms of pitch perception across animals.

Dual-pitch processing mechanisms in primate auditory cortex.

Pitch, our perception of how high or low a sound is on a musical scale, is a fundamental perceptual attribute of sounds and is important for both music and speech. After more than a century of research, the exact mechanisms used by the auditory system to extract pitch are still being debated. Theoretically, pitch can be computed using either spectral or temporal acoustic features of a sound. We have investigated how cues derived from the temporal envelope and spectrum of an acoustic signal are used for pitch extraction in the common marmoset (Callithrix jacchus), a vocal primate species, by measuring pitch discrimination behaviorally and examining pitch-selective neuronal responses in auditory cortex. We find that pitch is extracted by marmosets using temporal envelope cues for lower pitch sounds composed of higher-order harmonics, whereas spectral cues are used for higher pitch sounds with lower-order harmonics. Our data support dual-pitch processing mechanisms, originally proposed by psychophysicists based on human studies, whereby pitch is extracted using a combination of temporal envelope and spectral cues.

Learned vocalizations in budgerigars (Melopsittacus undulatus): the relationship between contact calls and warble song.

The budgerigar (Melopsittacus undulatus) has an extraordinarily complex, learned, vocal repertoire consisting of both the long rambling warble song of males and a number of short calls produced by both sexes. In warble, the most common elements (>30%) bear a strong resemblance to the highly frequency-modulated, learned contact calls that the birds produce as single utterances. However, aside from this apparent similarity, little else is known about the relationship between contact calls and warble call elements. Here, both types of calls were recorded from four male budgerigars. Signal analysis and psychophysical testing procedures showed that the acoustic features of these two vocalizations were acoustically different and perceived as distinctive vocalizations by birds. This suggests that warble call elements are not simple insertions of contact calls but are most likely different acoustic elements, created de novo, and used solely in warble. Results show that, like contact calls, warble call elements contain information about signaler identity. The fact that contact calls and warble call elements are acoustically and perceptually distinct suggests that they probably represent two phonological systems in the budgerigar vocal repertoire, both of which arise by production learning.

The effect of altered auditory feedback on control of vocal production in budgerigars (Melopsittacus undulatus).

Budgerigars learn their vocalizations by reference to auditory information and they retain the ability to learn new vocalizations throughout life. Auditory feedback of these vocalizations was manipulated in three experiments by training birds to produce vocalizations while wearing small earphones. Experiments 1 and 2 examined the effect of background noise level (Lombard effect) and the effect of manipulating feedback level from self-produced vocalizations (Fletcher effect), respectively. Results show that birds exhibit both a Lombard effect and a Fletcher effect. Further analysis showed that changes in vocal intensity were accompanied by changes in call fundamental frequency and duration. Experiment 3 tested the effect of delaying or altering auditory feedback during vocal production. Results showed subsequent production of incomplete and distorted calls in both feedback conditions. These distortions included changes in the peak fundamental frequency, amplitude, duration, and spectrotemporal structure of calls. Delayed auditory feedback was most disruptive to subsequent calls when the delay was 25 ms. Longer delays resulted in fewer errors.

Frequency discrimination in the common marmoset (Callithrix jacchus).

The common marmoset (Callithrix jacchus) is a highly vocal New World primate species that has emerged in recent years as a promising model system for studies of auditory and vocal processing. Our recent studies have examined perceptual mechanisms related to the pitch of harmonic complex tones in this species. However, no previous psychoacoustic work has measured marmosets' frequency discrimination abilities for pure tones across a broad frequency range. Here we systematically examined frequency difference limens (FDLs), which measure the minimum discriminable frequency difference between two pure tones, in marmosets across most of their hearing range. Results show that marmosets' FDLs are comparable to other New World primates, with lowest values in the frequency range of ∼3.5-14 kHz. This region of lowest FDLs corresponds with the region of lowest hearing thresholds in this species measured in our previous study and also with the greatest concentration of spectral energy in the major types of marmoset vocalizations. These data suggest that frequency discrimination in the common marmoset may have evolved to match the hearing sensitivity and spectral characteristics of this species' vocalizations.

An operant conditioning method for studying auditory behaviors in marmoset monkeys.

The common marmoset (Callithrix jacchus) is a small New World primate that has increasingly been used as a non-human model in the fields of sensory, motor, and cognitive neuroscience. However, little knowledge exists regarding behavioral methods in this species. Developing an understanding of the neural basis of perception and cognition in an animal model requires measurement of both brain activity and behavior. Here we describe an operant conditioning behavioral training method developed to allow controlled psychoacoustic measurements in marmosets. We demonstrate that marmosets can be trained to consistently perform a Go/No-Go auditory task in which a subject licks at a feeding tube when it detects a sound. Correct responses result in delivery of a food reward. Crucially, this operant conditioning task generates little body movement and is well suited for pairing behavior with single-unit electrophysiology. Successful implementation of an operant conditioning behavior opens the door to a wide range of new studies in the field of auditory neuroscience using the marmoset as a model system.

Measurement of absolute auditory thresholds in the common marmoset (Callithrix jacchus).

The common marmoset is a small, arboreal, New World primate that has emerged as a promising non-human model system in auditory neuroscience. A complete understanding of the neuroethology of auditory processing in marmosets will include behavioral work examining how sounds are perceived by these animals. However, there have been few studies of the marmoset's hearing and perceptual abilities and the audiogram of this species has not been measured using modern psychophysical methods. The present experiment pairs psychophysics with an operant conditioning technique to examine perception of pure tone stimuli by marmosets using an active behavioral paradigm. Subjects were trained to lick at a feeding tube when they detected a sound. Correct responses provided access to a food reward. Pure tones of varying intensities were presented to subjects using the method of constant stimuli. Behavioral thresholds were calculated for each animal based on hit rate--threshold was defined by the tone intensity that the animal correctly identified 50% of the time. Results show that marmoset hearing is comparable to that of other New World monkeys, with a hearing range extending from about 125 Hz up to 36 kHz and a sensitivity peak around 7 kHz.

Discrimination of auditory gratings in birds.

Auditory gratings (also called auditory ripples) are a family of complex, broadband sounds with sinusoidally modulated logarithmic amplitudes and a drifting spectral envelope. These stimuli have been studied both physiologically in mammals and psychophysically in humans. Auditory gratings share spectro-temporal properties with many natural sounds, including species-specific vocalizations and the formant transitions of human speech. We successfully trained zebra finches and budgerigars, using operant conditioning methods, to discriminate between flat-spectrum broadband noise and noises with ripple spectra of different densities that moved up or down in frequency at various rates. Results show that discrimination thresholds (minimum modulation depth) increased as a function of increasing grating periodicity and density across all species. Results also show that discrimination in the two species of birds was better at those grating periodicities and densities that are prominent in their species-specific vocalizations. Budgerigars were generally more sensitive than both zebra finches and humans. Both bird species showed greater sensitivity to descending auditory gratings, which mirrors the main direction in their vocalizations. Humans, on the other hand, showed no directional preference even though speech is somewhat downward directional. Overall, our results are suggestive of both common strategies in the processing of complex sounds between birds and mammals and specialized, species-specific variations on that processing in birds.