Sensitivity of the human temporal voice areas to nonhuman primate vocalizations

The study of cerebral mechanisms underlying speech and voice processing has gained importance since the early 2000s with the advent of functional magnetic resonance imaging (fMRI) (Ogawa et al., 1990). Voice-sensitive areas, commonly referred to as ‘temporal voice areas’ (TVAs) or simply ‘voice areas’, have been highlighted along the upper, superior portion of the temporal cortex (Belin et al., 2000). Since then, great efforts have been made to better characterize these TVA, with particular attention to their spatial division into functional subregions (Aglieri et al., 2018; Kriegstein and Giraud, 2004; Pernet et al., 2015). A fairly large body of literature points to the critical role of the TVA in voice perception and processing in healthy participants (Kriegstein and Giraud, 2004; Frühholz et al., 2020; Latinus and Belin, 2011; Zäske et al., 2017) as well as in lesioned patients (Roswandowitz et al., 2018). Subregions of the TVA have also been directly linked to social perception (Lahnakoski et al., 2012), vocal emotion processing (Ethofer et al., 2012; Witteman et al., 2012), voice identity (Latinus et al., 2011; Latinus et al., 2013), and gender perception (Charest et al., 2013). The developmental axis of voice processing has also been studied in infants, demonstrating the existence of the TVA and voice sensitivity in the human brain as early as 4 (Calce et al., 2024) and 7 (Grossmann et al., 2010) months of age, while the ability to respond specifically to the voice of their parents has been observed in fetuses in utero (Kisilevsky et al., 2003). With the ongoing development of brain imaging and analysis techniques (Hüppi, 2011), it is realistic to expect successful, albeit noninvasive, fMRI results on task-related voice perception in utero in the near future. Along the evolutionary axis, evidence for TVA or, more generally, conspecific vocalization-sensitive brain areas has emerged primarily in dogs (Andics et al., 2014), monkeys (Perrodin et al., 2011; Petkov et al., 2008) (Macaca mulatta) as well as recently in common marmosets (Dureux et al., 2025; Jafari et al., 2023) (Callithrix jacchus), raising the question of whether such specialized brain areas are species-specific (Fecteau et al., 2004) and to what extent human and nonhuman primates share neural mechanisms that enable them to preferentially process conspecific vocalizations (Belin, 2006). However, less attention has been paid to paradigms in which animal vocalizations are presented to humans—see Fecteau et al., 2004's study on species-specificity in the human brain. Human processing of animal vocalizations has been studied with both monkey and cat material, but no specific cross-species activations have been observed within the TVA with respect to either species (Belin et al., 2008a). Other studies have focused more specifically on phylogenetic distance and have included nonhuman ape (chimpanzee, Pan troglodytes) and ‘Old World’ monkey (rhesus macaque, M. mulatta) vocalizations as stimuli. Such studies failed to identify species-specific brain activations—despite correctly discriminating chimpanzee affective vocalizations (Fritz et al., 2018)—and observed ambivalent results for below (Fritz et al., 2018) vs. above (Linnankoski et al., 1994) chance discrimination of macaque affective vocalizations by human participants. A recent exception is a study in which functionally homologous anterior TVA activity was observed in both humans and macaques: this region was indeed specific to macaque calls in the macaque’s anterior TVA, and specific to human voices in the anterior TVA of humans, but no macaque-specific activity was observed in the human TVA (Bodin et al., 2021). Additionally, TVA responded similarly in both species to the presentation of nonverbal auditory stimuli, potentially due to some level of acoustic similarity (Bodin et al., 2021). This sparse literature motivated the present study, which aims to investigate cross-species TVA activations in humans when asked to categorize vocalizations from phylogenetically—and acoustically close and distant—species while undergoing fMRI scanning. While studies on the TVA typically involve passive listening, we wanted to additionally have the means to compare nonhuman primate species recognition/categorization in humans. The importance of acoustic differences between species and more specifically acoustic distance, particularly through fundamental frequency variations (Grawunder et al., 2018; Slocombe and Zuberbühler, 2007), was indeed of great interest. Acoustic distance—calculated using Mahalanobis distance with 16 acoustic parameters extracted from the stimuli, see Supplementary file 1A—was in fact a determining parameter in assessing affective cues recognition in nonhuman primate calls by human participants (Debracque et al., 2023). In this study, affiliative chimpanzee—but not bonobo—calls were acoustically the closest to positive human voice stimuli, suggesting a distinct evolution of bonobo calls (Debracque et al., 2023). Bonobo vocalizations are of particular interest because this species is thought to have undergone evolutionary changes in their communication, in part due to a neoteny process involving acoustic modifications, and although they are as phylogenetically close to humans as chimpanzees—with an estimated separation with the Homo lineage only 6–8 million years ago (Gruber and Clay, 2016). Previous research has shown that bonobos have a shorter larynx—a valid predictor of a species’ mean fundamental frequency (Titze et al., 2016)—compared to chimpanzees, resulting in a higher fundamental frequency in their calls (Grawunder et al., 2018). Such a difference has been demonstrated in juvenile bonobo calls compared to chimpanzee and human baby calls (Kelly et al., 2017), arguing for a greater acoustic distance between bonobo calls and human or chimpanzee vocalizations. For these reasons, we included vocalizations from both Pan species (chimpanzees, P. troglodytes; bonobos, Pan paniscus), as well as a phylogenetically more distant species (Cercopithecidae: rhesus monkeys), with an estimated separation with the Homo lineage dating back to 25 million years ago. Indeed, any claim of human ‘uniqueness’ for TVA selectivity remains on hold and should be tested in light of these closely related species. Using the same stimuli, we previously investigated the frontal mechanisms involved in the categorization of nonhuman primate vocalizations independently of a selection of low-level acoustic parameters (Ceravolo et al., 2023), but the possibility that acoustic differences would affect, at the auditory level, the ability of human participants to recognize nonhuman primate calls should be thoroughly examined, as we did in the present study. As suggested by research mentioned above, monkey vocalizations are overall less likely to be identified compared to ape vocalizations due to both phylogenetic and acoustic differences. Therefore, our mechanistic hypothesis of the difficulty for humans to recognize bonobo calls is that frequencies of the human tonotopic map in the auditory cortex—adapted and adjusted to the frequencies of the human voice during evolution—would not be tailored to process the frequencies generated by bonobo calls. It would also be the case for macaque calls, while frequencies of chimpanzee calls—being closer to the range of human voice fundamental frequency (Grawunder et al., 2018; Debracque et al., 2023)—would be better represented in the human auditory cortex and therefore more easily processed and better identified by humans.

According to the literature mentioned so far and to the mechanistic hypothesis underlying the processing of chimpanzee as opposed to bonobo and/or macaque calls by human participants, we therefore predicted: (1) Bioacoustics: more acoustic proximity between human and chimpanzee vocalizations, whereas more distance would separate those of bonobos and macaques from the human voice (Grawunder et al., 2018; Debracque et al., 2023; Cauzinille et al., 2024); (2) Phylogeny: a selectivity of the superior temporal lobe—within the TVA—for the processing of vocalizations from the Pan taxon (chimpanzee, bonobo) but not Cercopithecidae (rhesus monkey) vocalizations (Fecteau et al., 2004; Fritz et al., 2018; Gruber and Clay, 2016; Kelly et al., 2017; Debracque et al., 2025)—while considering acoustic features that characterize the stimuli the best through a discriminant analysis.

The present study provides evidence of the sensitivity of the human TVA to cross-species vocalizations, especially to chimpanzee calls but also to macaque vocalizations, as illustrated by selective enhanced activity in the bilateral mid and anterior STG and STS—within sample-specific TVA. We do not interpret these results as ‘absolute’ selectivity, but rather we emphasize the relative preference of these brain regions to chimpanzee and to a lesser extent macaque calls. These results were obtained through statistical modeling of the MRI data that included either simple acoustics or the use of Mahalanobis acoustic distance between species and the most discriminant acoustic features specific to our stimuli as covariates. These two latter analyses converged and yielded greatly overlapping results, especially in the anterior TVA. Therefore, our results suggest that vocalizations from another ape species recruit, or trigger activity in, subregions of human temporal cortex that process species-specific voices in humans—namely the bilateral, sample-specific TVA. This evidence speaks in favor of cross-species primate vocalization processing in the anterior and mid TVA of humans—for chimpanzee and macaque calls, respectively. Our results also suggest differential engagement of the TVA according to behavioral performance for species categorization. While our acoustic data confirmed the hypothesized hierarchy of acoustic distance as a function of phylogenetic distance between our species, we still observed mid STG and STS activity for macaque vs bonobo calls and a small cluster in the left mid STS selective to macaque calls in Model 3—an unexpected result since macaques are the most distant species from humans both phylogenetically and acoustically in our study. Therefore, while we initially hypothesized that primate calls would exclusively enhance activity in human TVA as a function of a combination of phylogenetic and acoustic proximity, our data also point toward the greater importance of the most discriminant acoustic features rather than acoustic distance alone. We discuss these aspects below in more detail and interpret their general meaning and subsequent scientific implications, in addition to highlighting the limitations of our study.

Often specifically associated with the processing of conspecific vocalizations (e.g., in humans Belin et al., 2000; Fecteau et al., 2004; Bodin et al., 2021), macaques (Petkov et al., 2008; Bodin et al., 2021; Perrodin et al., 2015), and dogs (Andics et al., 2014), the present study challenges the common view of the TVA as ‘species-specific’ and illustrates that human voices, chimpanzee, and macaque calls can enhance activity in the TVA. We think that the distinct locations of these TVA subregions recruited for processing the vocalizations of these primate species matters. In fact, there might be a possible association between anterior TVA—selective to processing chimpanzee calls—and the higher recognition performance of chimpanzee calls compared to those of bonobos or macaques in human participants (Ceravolo et al., 2023). Anterior TVA activity selective to the processing of chimpanzee calls occurred when these were compared to both human and nonhuman primate species, solely to other nonhuman primate vocalizations, or directly to the human voice. However, homologous results were not observed for bonobo, and they were more scarce—especially between models—for macaque vocalizations: we found macaque-selective activity in a small area of the planum temporale and in a small cluster of the left mid STS, congruent, for instance, with locations observed in the general processing of animal sounds, especially in the planum temporale (Engel et al., 2009; Lewis et al., 2005). On the other hand, within-TVA anterior STG activity was also observed when chimpanzee vocalizations were directly compared to the human voice. We think this result highlights the cross-species selectivity of this anterior subregion of the TVA for processing species phylogenetically close to humans and especially with human-like acoustics, namely the calls of chimpanzees in the case of our study. Because of their vocal proximity, the perception of human voices and chimpanzee calls in socio-affective contexts could involve a common ‘social’ core of the brain, which increases activity in brain regions such as the anterior TVA, as reported previously in studies pertaining to social contextual information processing in the anterior STG (Simmons et al., 2010; Zahn et al., 2007). Differences at the level of processing complexity between the two types of vocalizations could also explain this observation, while we demonstrated that saliency or attention-related effects do not exist between our species stimuli. Indeed, previous studies have shown the role of the anterior STG and the anterior STS in the conceptual representation of social context by the human voice (Simmons et al., 2010; Zahn et al., 2007; Bestelmeyer et al., 2011; Mellem et al., 2016). Therefore, our data might suggest that the anterior part of the superior temporal cortex could be recruited to process the social context of human and chimpanzee vocal stimuli. However, this processing would be more automated for the perception of the human voice than for chimpanzee calls because of our high exposure and expertise as humans to these vocal signals, but these hypotheses should be addressed scientifically in studies dedicated to this topic. Our results are also complementary to and coherent with a ‘voice patch’ system in the brain of primates, as put forward by Belin et al., 2018, and according to which distinct ‘patches’ or subregions of the temporal lobe—especially its anterior portion—would be interconnected and would allow for the processing of voice information. Such a system would be present in many primate species such as humans, macaques, and marmosets, with most recent evidence suggesting a population of neurons in the anterior STG of the macaque brain selective to human voice (Giamundo et al., 2024), as also anticipated in another study on macaques and also in the anterior STG (Perrodin et al., 2014). These fascinating and converging results mirror our present data—with chimpanzee calls triggering responses in the anterior STG/TVA of our human participants—and strongly emphasize the need for pursuing a comparative approach in order to clarify the cross-species neural bases underlying the processing of human and nonhuman primate vocal signals. As we mentioned previously, these interpretations are, considering our results, free of any potential attentional bias toward one species over the others, since no effect was observed on that matter in a control, behavioral study involving an independent sample of 28 participants in a species-specific exogenous cueing attentional paradigm—Methods and Figure 2—figure supplement 1.

Importantly, our data also emphasize the influence of acoustic features and especially acoustic proximity between human and chimpanzee vocalizations: we show that activity in the anterior STG and more generally in the anterior TVA partly depends on phylogenetic and, importantly, on key acoustic features—including acoustic proximity. Consistent with previous studies (Belin et al., 2008a; Fritz et al., 2018), we did not expect TVA activity for macaque calls processing because they are both phylogenetically and acoustically more distant from humans than the other species in this study—although, as mentioned above, we found a very small cluster in the left primary auditory cortex and mid STS for Model 3. It is interesting to note that in Model 2, with acoustic distance as trial-level covariate, we observed TVA activity only for chimpanzee but not macaque calls, giving further weight to the importance of acoustic distance in this context. On this matter, the mid STS location of the macaque-related cluster aligns with a cortical region preferentially responsive to non-rhythmic, ‘noise-like’ sounds—a category that acoustically includes macaque vocalizations—rather than to harmonic, voice-like signals (Norman-Haignere et al., 2019). This is further consistent with the posterior-to-anterior functional gradient of the superior temporal lobe, whereby mid and posterior regions process lower-level acoustic features and more anterior STG/STS regions support categorical sound recognition (Leaver and Rauschecker, 2010). Also, if only phylogenetic proximity mattered, bonobo calls should also elicit activity in the TVA because they are as phylogenetically close to humans as chimpanzees. But this viewpoint is rather reductive, and our results show that this is not entirely correct, and that activity in the TVA crucially depends on the acoustic properties of the perceived vocalizations since we cannot infer phylogeny from vocalizations. This interpretation is strongly supported by the inclusion of acoustic Mahalanobis distance for each species compared to the human voice as a trial-level covariate of no-interest. Using such modeling, differential neuroimaging results between chimpanzee and bonobo vocalizations were explained by both acoustic and phylogenetic proximity in the TVA. These results are consistent with the recent proposal—and recent findings (Debracque et al., 2023)—that there are substantial differences between chimpanzee and bonobo vocalizations. These encompass fundamental frequency range and mean due to larynx length (Grawunder et al., 2018; Titze et al., 2016)—despite the evolutionary relatedness to chimpanzees (Grawunder et al., 2018). Therefore, the interaction between phylogeny and acoustic distance or proximity would explain the anterior TVA expansion for processing specifically chimpanzee but not bonobo vocalizations. This argument, however, falls short to explain the activations of the TVA by macaque calls in Model 3, that may have been treated as less complex or structured sounds in the mid TVA (Norman-Haignere et al., 2019).

Overall, it seems reasonable to hypothesize that TVA activity is not per se human-specific (Belin et al., 2000; Bestelmeyer et al., 2011), but that TVA are instead sensitive to vocalizations from other primate species, provided that these vocalizations have sufficient acoustic proximity to human vocal signals—which would in itself be related to anatomical and/or behavioral changes throughout phylogenetic evolution. This integrative view is again consistent with the concept of a ‘voice patch’ system in the primate brain (Belin et al., 2018). We therefore propose that the mid and anterior TVA, unlike the rest of the TVA, would be heterospecific—sensitive to vocalization acoustics triggered by evolution. This proposition also implies a validation of our mechanistic hypothesis according to which the mean fundamental frequency of chimpanzee but not bonobo calls—the former being much closer to the mean fundamental frequency of the human voice (Grawunder et al., 2018), would allow for a better identification and recognition of chimpanzee calls by humans. This advantage would rely on neurons of the human auditory cortex—both the primary and more secondary regions—being specialized in the processing of low to mid fundamental frequencies such as those of the human voice and chimpanzee calls. In our third analysis model, we looked further into this aspect and included several acoustic properties of our stimuli as a function of the four species in our stimuli. A discriminant analysis (Debracque et al., 2023) allowed us to select specific acoustic features that best discriminate between our species stimuli. Namely, we took the six parameters explaining the most the differences between our stimuli, including vocalization loudness, intensity—similar to our ‘energy’ covariate of Model 1, in addition to change in spectrum, F2 bandwidth contour, F0 power, and intensity contour difference. Using these more sophisticated acoustic features as covariates of no-interest, we still obtained brain imaging results very similar to those of Model 1 and even closer to Model 2—with acoustic distance as covariate, yet with some subtle differences in anterior STG cluster size and location. The peaks were indeed located more ventral and were larger—as compared to results of Models 1 and 2, especially for the processing of chimpanzee- and macaque-selective vocalizations compared to all primate species and to nonhuman primates alone. These results suggest that the inclusion of spectrum change to intensity- and frequency-related acoustical parameters of the vocal signals slightly shifted and enlarged activation locations in the anterior STG. This result is again congruent with the proposed existence of ‘voice patches’ in the temporal lobe of primate species (Belin et al., 2018), with the interconnectivity of these patches highly depending on very fine-grained acoustic aspects of primate vocal signals. This step motivated the inclusion of these parameters as covariates of no-interest in neuroimaging Model 3, to retain brain activations marginally independent of such acoustics. The congruence between these data should be explored in more detail in the future by the combination of computational bioacoustics and functional neuroimaging, due to the high relevance and sensitivity of combining these techniques to investigate primate social communication (Cauzinille et al., 2024).

A final but maybe more secondary interpretation arising from our results regarding bonobo calls also supports the evolutionary divergence of this peculiar species. According to the self-domestication hypothesis, bonobos would have evolved differently than chimpanzees due to selection against aggression (Hare et al., 2012). Interestingly, differentiation in the evolutionary path of bonobos has influenced both their behavior (Gruber and Clay, 2016) and morphology, leading to differences at the level of call production (Grawunder et al., 2018; Kelly et al., 2017). Considering these documented acoustic differences and putting them in perspective with our neuroimaging data, the calls of our last common ancestor with the other Pan species 8 million years ago (Perelman et al., 2011), may have been closer to those uttered by modern chimpanzees than to those of bonobos. Our data indeed show that modern human brains remain more sensitive to the acoustic characteristics of the calls of the former compared to the latter, arguing for more conserved calls between modern chimpanzees and humans. This aspect is also in line with significant differences between, for instance, the fundamental frequency of human baby cries or babbling (~250–600 Hz) compared to that of bonobos (~1000–3500 Hz) (Dewi et al., 2019; Jagtap et al., 2016), while they correspond more closely to the fundamental frequency of chimpanzee calls (~500–1000 Hz) (Grawunder et al., 2018). In our study, bonobo calls definitely are so much different than those uttered by the species of our other stimuli, that they presumably fall outside of the phylogeny and acoustic proximity factors that we outlined so far. This would also put into perspective the selectivity of mid TVAs for macaque calls. The distinct analysis we computed, dedicated to acoustic differences between chimpanzee and bonobo calls, highlighted specificities in pitch dynamics, phonation quality—periodicity, breathiness, glottal irregularity—and vocal tract resonance. This analysis therefore revealed the more stable, lower-pitched, periodically structured nature of the calls of chimpanzees relative to the higher, breathier, and more variable calls of bonobos. These data align well with those obtained through Mahalanobis acoustic distance data discussed above, again converging toward voice-like acoustics for chimpanzee calls.

In a sense, we therefore validate our first hypothesis regarding the existence of acoustic distance between each primate species used in our study. We also partially validate our second hypothesis, albeit not completely. In fact, macaque compared to bonobo or other primate calls in Model 3 revealed mid TVA activations, and we think that these activations may depend specifically on the importance of the most discriminant acoustic features. Several TVA subregions or ‘patches’ underlying cross-species primate vocalization processing might therefore exist, and our data highlight at least one of them in the mid and anterior portion of the TVA.

Behavioral data should also be discussed in the context of the species categorization task. We know from our attentional control task that species categorization was not biased by greater saliency from a specific species. We can therefore consider the proportion of correct categorization as attention-bias free in that regard. A ceiling effect was expected and observed for human voice, while only chimpanzee and macaque vocal signals were categorized above chance level for nonhuman primate species. Interestingly, no difference was observed in accuracy between these two, while bonobo calls were categorized below chance. These results are at odds with the acoustic distance argument per se, since we show that macaque coos are the furthest from human voice and yet these were better recognized than acoustically closer bonobo calls. The neural correlates of species categorization performance also point toward the calls of bonobos being completely different than the other species, recruiting most TVA territory compared to other species. Combined, and aligning with previous data (Debracque et al., 2023; Ceravolo et al., 2023; Debracque et al., 2025), these puzzling behavioral and neural results illustrate the very different nature of bonobo calls, and the fact that acoustically, they may have even represented an ‘object’ that was not part of the primate category for our participants. Considering the vast TVA activations compared to the other species, bonobos calls were also most probably very engaging, congruent with massive resources being allocated due to hesitation and decisional difficulty (Ceravolo et al., 2023).

Considering behavioral data and acoustics, we should also mention the possibility that familiarity to some species may have influenced our results. In fact, differential familiarity with the stimulus species through media or zoo exposure cannot be entirely ruled out. However, this interpretation is undermined by the observation that bonobo calls failed to elicit any anterior TVA response. This interpretation also suffers from the fact that bonobos are phylogenetically equidistant from humans as chimpanzees, and are equally unfamiliar to Western participants, although maybe less culturally present than chimpanzees. Consistent with this nuanced viewpoint, ERP evidence suggests that early, automatic neural responses to primate vocalizations are modulated by phylogenetic proximity rather than familiarity—with the latter influencing only later attentional processing stages (Scheumann et al., 2014; Scheumann et al., 2017).

A fundamental challenge, shared by vocal science, cognitive and affective neuroscience fields, relates to dissociating biologically relevant information from acoustic properties: species-specific vocal signals are in fact entirely instantiated in acoustics—there is no ‘non-acoustic’ biological residual in the strict sense (Debracque et al., 2023; Cauzinille et al., 2024; Leaver and Rauschecker, 2010). Our Models 1–3 therefore demonstrate independence from specific, theory-motivated parameterizations of the acoustic signal rather than from acoustic information in its entirety. Therefore, residual anterior TVA response to chimpanzee calls most plausibly reflects sensitivity to higher-order acoustic structure not captured—at least not entirely—by these lower-dimensional features. This higher-order acoustic structure may include patterns of spectro-temporal properties of species-typical calls, their sequential organization, or the results could also depend on an evolutionary ‘tuning’ of the human anterior TVA to an acoustic processing niche shared with the great ape vocal system (Belin et al., 2018). We acknowledge this as a fundamental limitation of the acoustic-control approach in comparative vocal neuroimaging, and in our study, and suggest that encoding models using richer spectro-temporal representations—such as, for instance, more complex sequences of calls rather than single bursts—may offer more exhaustive acoustic control in future work.

Therefore, even though we tried to control for critical acoustic features, species categories, and their related evolutionary distance, several limitations should be mentioned. These limitations are both theoretical and methodological. First, we cannot rule out the fact that including more primate species in our set of stimuli would have influenced the results. In fact, even though our species categories were specifically chosen for this task, the inclusion of vocalizations from other great apes—such as gorillas or orangutans—would have broadened the scope of our results. Related to this aspect, we can also mention that tackling primate phylogeny, which spans over millions of years, with only four species restricts the possible inference based on our results. Also, not including either nonvocal stimuli or scrambled nonhuman primate calls limits the interpretability of the results, since we cannot rule out that the auditory species ‘object’ per se was triggering the results. Active species categorization compared to passive listening may also introduce a decision-making bias in the neural effects observed. In fact, we observed improved sensitivity of our data by the use of more sophisticated acoustic modeling, namely the inclusion of both between-species acoustic distance and of the most discriminant acoustic features in the functional imaging data. However, we did not include as stimuli—or in a control task—the synthesized acoustic parameters of interest, for instance, by using species-specific F0 contour or its spectral content in other neutral, comparable auditory stimuli. We cannot therefore completely rule out that such tasks would not trigger brain activations that overlap with our results—although such data would not be mutually exclusive with our data and interpretation. Future work should therefore address with the greatest level of detail the specific question of acoustics in primate vocalization processing, in addition to adding more—as well as synthesized—stimuli from other great ape species, and if possible using both bursts as well as more complex sequences of calls. The origin of these acoustic differences should also be investigated, since we can assume that these differences originated at least partially from evolutionary processes as well as survival and adaptation mechanisms. Linked to this aspect, phylogeny and acoustics were at least partly confounded in our factorial design, and using dedicated synthetic vs natural vocal material as stimuli would disentangle this issue. Setting the acoustic covariates to zero in the fMRI models also did not inform on the impact of having acoustics of interest, and this aspect should be studied in the future. Finally, individual differences in the processing and preference of one species over another or over all the others cannot be ruled out, even though we provide evidence that attentional effects toward the vocalizations of a specific species did likely not exist in our data. Therefore, individual differences should be assessed in more detail in the future, with the inclusion of participant-level covariates such as questionnaire scores assessing the familiarity with primate vocalizations or the hedonic value of these vocalizations for each individual. Among the more general limitations of nonhuman primate neuroscience lies the fact that more inclusive and large-scale collaborations would be needed. Such collaborations and frameworks would lead to a better study and understanding of primate neuroscience, and previous initiatives have recently been put forward in this direction (Hartig et al., 2023; Milham et al., 2022).

Taken together, our data suggest that phylogeny-driven specific acoustic features appear to be necessary to trigger cross-species activity in the human TVAs—especially in subregions of the TVA in which increased activity underlies voice signals compared to animal and nature sounds. We provide evidence for specific anterior and mid TVA subregions that underlie the processing of the calls of one of our closest relatives, namely chimpanzees but also of macaques, respectively. In line with recently reported literature, we contend that the human TVA are also involved in the processing of heterospecific primate vocalizations, provided they exhibit sufficient phylogenetic and especially spectro-temporal acoustic proximity to the human voice; as such, we predict that other similarities will be uncovered in the processing of human and nonhuman primate communicative signals. Finally, our results support a critical evolutionary continuity between the structure of human and chimpanzee vocalizations, possibly reflecting one of their common ancestors, as opposed to bonobo vocalizations that underwent more recent and critical changes within the last 1–2 million years. In contrast, the chimpanzee vocal system may be closer to that of the common ancestors of humans and chimpanzees, as shown by the conserved activation in the human modern brain.

All data, stimuli, and codes used in this article are available in the FAIR-compliant open repository YARETA (URL: https://doi.org/10/g8wkrb).

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Author details

1. Leonardo Ceravolo

   University of Geneva, Geneva, Switzerland

   Contribution

   Conceptualization, Data curation, Software, Formal analysis, Validation, Investigation, Visualization, Methodology, Writing – original draft, Writing – review and editing

   Contributed equally with

   Coralie Debracque

   For correspondence

   Leonardo.Ceravolo@unige.ch

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0003-0638-3981

2. Coralie Debracque

   University of Geneva, Geneva, Switzerland

   Contribution

   Conceptualization, Data curation, Validation, Investigation, Writing – original draft, Writing – review and editing

   Contributed equally with

   Leonardo Ceravolo

   Competing interests

   No competing interests declared

3. Thibaud Gruber

   University of Geneva, Geneva, Switzerland

   Contribution

   Resources, Supervision, Funding acquisition, Validation, Project administration, Writing – review and editing

   Contributed equally with

   Didier Grandjean

   Competing interests

   No competing interests declared

4. Didier Grandjean

   University of Geneva, Geneva, Switzerland

   Contribution

   Resources, Supervision, Funding acquisition, Validation, Project administration, Writing – review and editing

   Contributed equally with

   Thibaud Gruber

   Competing interests

   No competing interests declared

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  citation for Reviewed Preprint v1 https://doi.org/10.7554/eLife.108795.1