Acoustic Features of Rhesus Vocalizations and Their Representation in the Ventrolateral Prefrontal Cortex

Abstract

tion is one of the fundamental components of both human and nonhuman animal behavior. Auditory communication signals (i.e., vocalizations) are especially important in the socioecology of several species of nonhuman primates such as rhesus monkeys. In rhesus, the ventrolateral prefrontal cortex (vPFC) is thought to be part of a circuit involved in representing vocalizations and other auditory objects. To further our understanding of the role of the vPFC in processing vocalizations, we characterized the spectrotemporal features of rhesus vocalizations, compared these features with other classes of natural stimuli, and then related the rhesus-vocalization acoustic features to neural activity. We found that the range of these spectrotemporal features was similar to that found in other ensembles of natural stimuli, including human speech, and identified the subspace of these features that would be particularly informative to discriminate between different vocalizations. In a first neural study, however, we found that the tuning properties of vPFC neurons did not emphasize these particularly informative spectrotemporal features. In a second neural study, we found that a first-order linear model (the spectrotemporal receptive field) is not a good predictor of vPFC activity. The results of these two neural studies are consistent with the hypothesis that the vPFC is not involved in coding the first-order acoustic properties of a stimulus but is involved in processing the higher-order information needed to form representations of auditory objects. I N T R O D U C T I O NCommunication is one of the fundamental components of both human and nonhuman animal behavior (Hauser 1997). Although the benefits and importance of language in human evolution are obvious (Carruthers 2002;Hauser 1997;Lieberman 2002), other nonhuman communication systems are also important. These communication systems are important because for most, if not all, species they are critical to the species' survival (Andersson 1996;Bennett et al. 1997;Greenfield 2002;Hauser 1997;Lau et al. 2000;Mech and Boitani 2003).For example, auditory communication signals (i.e., speciesspecific vocalizations) are especially important in the socioecology of several species of nonhuman primates (Cheney and Seyfarth 1985;Eimas 1994;Eimas et al. 1971;Hauser 1997;Jusczyk 1997;Jusczyk et al. 1983; Miller and Eimas 1995), such as rhesus monkeys (Macaca mulatta). Vocalizations convey information about the identity and the age of the caller and often provide information about sex and emotional or motivational state (Cheney and Seyfarth 1990; Hauser 1997). Some vocalizations transmit information about objects and events in the environment (Gifford 3rd et al. 2003;Hauser 1998;Seyfarth and Cheney 2003).In rhesus monkeys, the ventrolateral prefrontal cortex (vPFC) plays an important role in processing vocalizations (Hackett et al. 1999;Romanski and Goldman-Rakic 2002;Romanski et al. 1999 Romanski et al. , 2005. The vPFC is thought to be part of a circuit involved in representing au...

Processing of emotional vocalizations in bilateral inferior frontal cortex

“…Future studies should investigate which features drive the discrimination and categorization abilities of the IFC. According to nonhuman primate studies, the IFC is rather sensitive to higherorder acoustic information (complex object representations) instead of first-order acoustic properties (simple spectro-temporal features) in vocalizations (Cohen et al, 2007). However, discrimination and categorization of vocal expressions depends on specific features (Banse and Scherer, 1996;Lakshminarayanan et al, 2003;Sauter et al, 2010).…”

“…Instead of low-level auditory features, these neurons seem to Single cell activity was usually recorded in BA 45A and BA 9/46v, both located rostrally to BA 8Av below the principal sulcus. Color-coded dots refer to the following studies: (Gifford et al, 2005), Romanski et al, 2005), (Cohen et al, 2007Russ et al, 2008a), (Romanski and Goldman-Rakic, 2002), (Cohen et al, 2006), (Lee et al, 2009;Russ et al, 2008b), (Sugihara et al, 2006), and (Gil-da-Costa et al, 2006) for activity in the vPM. Abbreviations: as arcuate sulcus, cs central sulcus, ipd inferior precentral dimple, ls lateral sulcus, ps principal sulcus, vpm ventral premotor area.…”

“…Abbreviations: as arcuate sulcus, cs central sulcus, ipd inferior precentral dimple, ls lateral sulcus, ps principal sulcus, vpm ventral premotor area. decode higher-order information conveyed by those vocalizations (Cohen et al, 2007). This decoding is probably based on a sensitivity to the acoustic morphology of conspecific vocalizations (Romanski et al, 2005), which help to differentiate several types of vocalizations (Cohen et al, 2006Gifford et al, 2005;Russ et al, 2008b).…”

Neural processing of natural sounds

“…azimuthal location) and such responses have been found in secondary mammalian and avian auditory areas [91,92]. In terms of higher-level categorization, research in starlings points to a role of the Caudio-Medial Nidopallium (NCM) for classifying behaviorally relevant classes of songs [93] and research in primates suggests that both the Superior Temporal Gyrus (STG) and the ventrolateral Prefontral Cortex (vPFC) could be involved in semantic discrimination [94][95][96][97][98]. Similar cortical areas have been shown in a large body of research to be critical for human speech processing [99].…”

An Auditory Region in the Primate Insular Cortex Responding Preferentially to Vocal Communication Sounds

“…Importantly, in several cases, different degrees of auditory agnosia, the inability to recognize sounds, have been well documented (Hyman and Tranel, 1989;Engelien et al, 1995;Griffiths et al, 1997). Noteworthy, neurons selective to conspecific vocalizations have also been reported at other stages of auditory processing, such as in the ventro-lateral prefrontal cortex (Romanski et al, 2005;Cohen et al, 2007), the superior temporal gyrus (Russ et al, 2008) and in the auditory cortex (Tian et al, 2001;Kikuchi et al, 2007;Recanzone, 2008). This suggests that selectivity to vocalizations is present at multiple stages of acoustic analysis, possibly reflecting the behavioral importance of these sounds.…”