Organisms that use vocal signals to communicate often modulate their vocalizations to avoid being masked by other sounds in the environment. Although some environmental noise is continuous, both biotic and abiotic noise can be intermittent, or even periodic. Interference from intermittent noise can be avoided if calls are timed to coincide with periods of silence, a capacity that is unambiguously present in insects, amphibians, birds, and humans. Surprisingly, we know virtually nothing about this fundamental capacity in nonhuman primates. Here we show that a New World monkey, the cotton-top tamarin (Saguinus oedipus), can restrict calls to periodic silent intervals in loud white noise. In addition, calls produced during these silent intervals were significantly louder than calls recorded in silent baseline sessions. Finally, average call duration dropped across sessions, indicating that experience with temporally patterned noise caused tamarins to compress their calls. Taken together, these results show that in the presence of a predictable, intermittent environmental noise, cotton-top tamarins are able to modify the duration, timing, and amplitude of their calls to avoid acoustic interference.

The Lombard effect-an increase in vocalization amplitude in response to an increase in background noise-is observed in a wide variety of animals. We investigated this basic form of vocal control in the cotton-top tamarin (Saguinus oedipus) by measuring the amplitude of a contact call, the combination long call (CLC), while simultaneously varying the background noise level. All subjects showed a significant increase in call amplitude and syllable duration in response to an increase in background noise amplitude. Together with prior results, this study shows that tamarins have greater vocal control in the context of auditory feedback perturbation than previously suspected.

Auditory feedback is critical for the development and maintenance of speech in humans. In contrast, studies of nonhuman primate vocal production generally report that subjects show little reliance on auditory input. We examined the extent to which cotton-top tamarin (Saguinus oedipus) vocal production is sensitive to perturbation of auditory feedback by manipulating the predictability of presentation of a 1 s burst of white noise during the production of the species-specific contact call, the combination long call (CLC). We used three experimental conditions: the Begin condition, in which white noise was presented only during the first half of a recording session, the End condition, in which white noise was presented only in the last half, and the Random condition, in which each call had a 50% probability of receiving white noise playback throughout the recording session, making the auditory feedback unpredictable. In addition we recorded calls before and after the experimental series (Baseline condition) to determine whether any changes induced by modification of auditory feedback persisted. Results showed that playback of white noise during the production of the CLC produced changes in the temporal structure of the CLC: calls were shorter and had fewer pulses, indicating that modification of auditory feedback can interrupt vocal production. In addition, calls that received modified feedback were louder and had longer inter-pulse intervals than those that did not, consistent with an adaptive response to the masking effect of white noise playback. The magnitude of this compensatory effect and the interruption rate were both sensitive to whether the feedback modification occurred at the beginning or end of the experimental session: early feedback produced less interruption and more compensation. Finally, when auditory feedback modification was unpredictable, adaptive changes were observed in both calls that received modified feedback and those that received normal feedback, suggesting that tamarins can generate an expectation of noise playback and increase vocal amplitude in anticipation of masking.

The importance of auditory feedback in the development of spoken language in humans is striking. Paradoxically, although auditory-feedback-dependent vocal plasticity has been shown in a variety of taxonomic groups, there is little evidence that our nearest relatives–non-human primates–require auditory feedback for the development of species-typical vocal signals. Because of the apparent lack of developmental plasticity in the vocal production system, neuroscientists have largely ignored the neural mechanisms of non-human primate vocal production and perception. Recently, the absence of evidence for vocal plasticity from developmental studies has been contrasted with evidence for vocal plasticity in adults. We argue that this new evidence makes non-human primate vocal behavior an attractive model system for neurobiological analysis.

The interaural time difference (ITD) is a major cue to sound localization along the horizontal plane. The maximum natural ITD occurs when a sound source is positioned opposite to one ear. We examined the ability of owls and humans to detect large ITDs in sounds presented through headphones. Stimuli consisted of either broad or narrow bands of Gaussian noise, 100 ms in duration. Using headphones allowed presentation of ITDs that are greater than the maximum natural ITD. Owls were able to discriminate a sound leading to the left ear from one leading to the right ear, for ITDs that are 5 times the maximum natural delay. Neural recordings from optic-tectum neurons, however, show that best ITDs are usually well within the natural range and are never as large as ITDs that are behaviorally discriminable. A model of binaural crosscorrelation with short delay lines is shown to explain behavioral detection of large ITDs. The model uses curved trajectories of a cross-correlation pattern as the basis for detection. These trajectories represent side peaks of neural ITD-tuning curves and successfully predict localization reversals by both owls and human subjects.

The effect of binaural decorrelation on the processing of interaural level difference cues in the barn owl (Tyto alba) was examined behaviorally and electrophysiologically. The electrophysiology experiment measured the effect of variations in binaural correlation on the first stage of interaural level difference encoding in the central nervous system. The responses of single neurons in the posterior part of the ventral nucleus of the lateral lemniscus were recorded to stimulation with binaurally correlated and binaurally uncorrelated noise. No significant differences in interaural level difference sensitivity were found between conditions. Neurons in the posterior part of the ventral nucleus of the lateral lemniscus encode the interaural level difference of binaurally correlated and binaurally uncorrelated noise with equal accuracy and precision. This nucleus therefore supplies higher auditory centers with an undegraded interaural level difference signal for sound stimuli that lack a coherent interaural time difference. The behavioral experiment measured auditory saccades in response to interaural level differences presented in binaurally correlated and binaurally uncorrelated noise. The precision and accuracy of sound localization based on interaural level difference was reduced but not eliminated for binaurally uncorrelated signals. The observation that barn owls continue to vary auditory saccades with the interaural level difference of binaurally uncorrelated stimuli suggests that neurons that drive head saccades can be activated by incomplete auditory spatial information.

Humans respond adaptively to uncertainty by escaping or seeking additional information. To foster a comparative study of uncertainty processes, we asked whether humans and a bottlenosed dolphin (Tursiops truncatus) would use similarly a psychophysical uncertain response. Human observers and the dolphin were given 2 primary discrimination responses and a way to escape chosen trials into easier ones. Humans escaped sparingly from the most difficult trials near threshold that left them demonstrably uncertain of the stimulus. The dolphin performed nearly identically. The behavior of both species is considered from the perspectives of signal detection theory and optimality theory, and its appropriate interpretation is discussed. Human and dolphin uncertain responses seem to be interesting cognitive analogs and may depend on cognitive or controlled decisional mechanisms. The capacity to monitor ongoing cognition, and use uncertainty appropriately, would be a valuable adaptation for animal minds. This recommends uncertainty processes as an important but neglected area for future comparative research.