The Role of Temporal Cues in Rhesus Monkey Vocal Recognition: Orienting Asymmetries to Reversed Calls

Abstract

An understanding of the acoustic cues that animals use to categorize their vocalizations has important implications for the way we design neuroethological investigations of auditory function. Compared to other species, we know relatively little about the kinds of acoustic features used by nonhuman primates to recognize and categorize vocalizations. To further our understanding, this study explores the role of temporal features in recognition of conspecific vocalizations by rhesus macaques (Macaca mulatta). Experiments were designed to extend an earlier set of findings showing that adult rhesus macaques selectively turn with the right ear leading when a conspecific vocalization is played 180° behind them, but turn left or not at all when a non-conspecific signal is played. Two call types were used as stimuli: shrill barks (alarm call) and harmonic arches (food call). We found that for normal calls, rhesus macaques turned to the right – supporting earlier findings – but for time- reversed shrill barks and harmonic arches, subjects oriented to the left. These results suggest that for at least a subset of calls, rhesus macaques use temporal cues to recognize conspecific vocal signals. The asymmetry of the behavioral response, and the corresponding asymmetry in the time-amplitude waveform, may have important implications for studies of temporal coding in the primate auditory system.

Right ear advantage for vocal communication in frogs results from both structural asymmetry and attention modulation

“…Accordingly, language lateralization in humans may reflect a more primitive left-hemispheric dominance for processing basic features of species-typical sounds [16] in which temporal features might be determinant auditory cues for call recognition. This theory is consistent with the results of experiments utilizing time reversed call playbacks in rhesus macaques and dogs resulting in a shift from right-ear to left-ear bias [62,63].…”

Wernicke's area homologue in chimpanzees (Pan troglodytes) and its relation to the appearance of modern human language

“…Recently, Gannon et al (2008) demonstrated asymmetry of area Tpt volume in macaque monkeys, with five of six macaque brains displaying a leftward bias. Congruent with these anatomical findings, several studies of non-human primates have revealed a right ear orienting bias when subjects are presented with species-specific vocal calls (Petersen et al 1978;Beecher et al 1979;Hauser & Anderson 1994;Hauser et al 1998;Ghazanfar et al 2001), suggesting left hemisphere specialization for processing communication signals. Similarly, experimental lesion of the left superior temporal cortex in Japanese macaques results in transient disruption of the ability to discriminate conspecific vocalizations, whereas there is no such deficit with right hemisphere lesion (Heffner & Heffner 1984).…”

Probabilistic Encoding of Vocalizations in Macaque Ventral Lateral Prefrontal Cortex

“…These studies have demonstrated that, for example, the interpulse interval in noisy calls as well as the temporal direction of the calls can be relevant for call discrimination Ghazanfar et al, 2001a). Such features are well modeled by the HMMs because the duration of the interpulse interval can be modeled by how long the HMM would remain in a state related to the interpulse interval, and as such, if this interval was shortened, the HMM could detect the call as no longer coming from the appropriate class.…”

“…If a feature is not useful for distinguishing among the classes of calls, it would not be a useful feature for the auditory system to encode for the purpose of call discrimination. Behavioral research suggests that primates use multiple features to discriminate among calls, including the interpulse interval in noisy calls, the overall amplitude envelope and the location of inflections in the frequency contour Le Prell and Moody, 2000;Ghazanfar et al, 2001aGhazanfar et al, , 2002. Previous research on the primate auditory cortex suggests that the frequency (Barbour and Wang, 2003) or temporal contrast of sounds is being represented.…”