Sensitivity of the human temporal voice areas to nonhuman primate vocalizations
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eLife Assessment
This valuable study shows that regions of the human auditory cortex that respond strongly to voices are also sensitive to vocalizations from closely related primate species. The study is methodologically solid, though additional analyses - particularly those isolating the acoustic features that differentiate chimpanzee from bonobo calls - would further strengthen the conclusions. With additional analyses and discussions, the work has the potential to offer key insights into the evolutionary continuity of voice processing and would be of interest to researchers studying auditory processing and evolutionary neuroscience in general.
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Abstract
In recent years, research on voice processing in the human brain—particularly the study of temporal voice areas (TVA)—was dedicated almost exclusively to conspecific vocalizations. To characterize commonalities and differences regarding primate vocalization representations in the human brain, the inclusion of closely related nonhuman primates—namely chimpanzees and bonobos—is needed. We hypothesized that neural commonalities would depend on both phylogenetic and acoustic proximities, with chimpanzees ranking closest to Homo. Presenting human participants (N=23) with the vocalizations of four primate species (rhesus macaques, chimpanzees, bonobos and humans) and regressing-out relevant acoustic parameters using three distinct analyses, we observed within-TVA, sample-specific, bilateral anterior superior temporal gyrus activity for chimpanzee vocalizations compared to: all other species; nonhuman primates; human vocalizations. Within-TVA activity was also observed for macaque vocalizations. Our results provide evidence for subregions of the TVA that respond principally—but not exclusively—to phylogenetically and acoustically close nonhuman primate vocalizations, namely those of chimpanzees.
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eLife Assessment
This valuable study shows that regions of the human auditory cortex that respond strongly to voices are also sensitive to vocalizations from closely related primate species. The study is methodologically solid, though additional analyses - particularly those isolating the acoustic features that differentiate chimpanzee from bonobo calls - would further strengthen the conclusions. With additional analyses and discussions, the work has the potential to offer key insights into the evolutionary continuity of voice processing and would be of interest to researchers studying auditory processing and evolutionary neuroscience in general.
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Reviewer #1 (Public review):
Summary:
This study investigates how human temporal voice areas (TVA) respond to vocalizations from nonhuman primates. Using functional MRI during a species-categorization task, the authors compare neural responses to calls from humans, chimpanzees, bonobos, and macaques while modeling both acoustic and phylogenetic factors. They find that bilateral anterior TVA regions respond more strongly to chimpanzee than to other nonhuman primate vocalizations, suggesting that these regions are sensitive not only to human voices but also to acoustically and evolutionarily related sounds.
The work provides important comparative evidence for continuity in primate vocal communication and offers a strong empirical foundation for modeling how specific acoustic features drive TVA activity.
Strengths:
(1) Comparative scope: …
Reviewer #1 (Public review):
Summary:
This study investigates how human temporal voice areas (TVA) respond to vocalizations from nonhuman primates. Using functional MRI during a species-categorization task, the authors compare neural responses to calls from humans, chimpanzees, bonobos, and macaques while modeling both acoustic and phylogenetic factors. They find that bilateral anterior TVA regions respond more strongly to chimpanzee than to other nonhuman primate vocalizations, suggesting that these regions are sensitive not only to human voices but also to acoustically and evolutionarily related sounds.
The work provides important comparative evidence for continuity in primate vocal communication and offers a strong empirical foundation for modeling how specific acoustic features drive TVA activity.
Strengths:
(1) Comparative scope: The inclusion of four primate species, including both great apes and monkeys, provides a rare and valuable cross-species perspective on voice processing.
(2) Methodological rigor: Acoustic and phylogenetic distances are carefully quantified and incorporated into the analyses.
(4) Neuroscientific significance: The finding of TVA sensitivity to chimpanzee calls supports the view that human voice-selective regions are evolutionarily tuned to certain acoustic features shared across primates.
(4) Clear presentation: The study is well organized, the stimuli well controlled, and the imaging analyses transparent and replicable.
(5) Theoretical contribution: The results advance understanding of the neural bases of voice perception and the evolutionary roots of voice sensitivity in the human brain.
Weaknesses:
(1) Acoustic-phylogenetic confound: The design does not fully disentangle acoustic similarity from phylogenetic proximity, as species co-vary along both dimensions. A promising way to address this would be to include an additional model focusing on the acoustic features that specifically differentiate bonobo from chimpanzee calls, which share equal phylogenetic distance to humans.
(2) Selectivity vs. sensitivity: Without non-vocal control sounds, the study cannot determine whether TVA responses reflect true selectivity for primate vocalizations or general auditory sensitivity.
(3) Task demands: The use of an active categorization task may engage additional cognitive processes beyond auditory perception; a passive listening condition would help clarify the contribution of attention and task performance.(4) Figures and presentation: Some results are partially redundant; keeping only the most representative model figure in the main text and moving others to the Supplementary Material would improve clarity.
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Reviewer #2 (Public review):
Summary:
This study investigated how the human brain responds to vocalizations from multiple primate species, including humans, chimpanzees, bonobos, and rhesus macaques. The central finding - that subregions of the temporal voice areas (TVA), particularly in the bilateral anterior superior temporal gyrus, show enhanced responses to chimpanzee vocalizations - suggests a potential neural sensitivity to calls from phylogenetically close nonhuman primates.
Strengths:
The authors employed three analytical models to consistently demonstrate activation in the anterior superior temporal gyrus that is specific to chimpanzee calls. The methodology was logical and robust, and the results supporting these findings appear solid.
Weakness:
The interpretation of the findings in this paper regarding the evolutionary …
Reviewer #2 (Public review):
Summary:
This study investigated how the human brain responds to vocalizations from multiple primate species, including humans, chimpanzees, bonobos, and rhesus macaques. The central finding - that subregions of the temporal voice areas (TVA), particularly in the bilateral anterior superior temporal gyrus, show enhanced responses to chimpanzee vocalizations - suggests a potential neural sensitivity to calls from phylogenetically close nonhuman primates.
Strengths:
The authors employed three analytical models to consistently demonstrate activation in the anterior superior temporal gyrus that is specific to chimpanzee calls. The methodology was logical and robust, and the results supporting these findings appear solid.
Weakness:
The interpretation of the findings in this paper regarding the evolutionary continuity of voice processing lacks sufficient evidence. A simple explanation is that the observed effects can be attributed to the similarity in low-level acoustic features, rather than effects specific to phylogenetically close species. The authors only tested vocalizations from three non-human primate species, other than humans. In this case, the species specificity of the effect does not fully represent the specificity of evolutionary relatedness.
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Reviewer #3 (Public review):
Summary:
Ceravolo et al. employed functional magnetic resonance imaging (fMRI) to examine how the temporal voice areas (TVA) in the human brain respond to vocalizations from different nonhuman primate species. Their findings reveal that the human TVA is not only responsible for human vocalizations but also exhibits sensitivity to the vocalizations of other primates, particularly chimpanzee vocalizations sharing acoustic similarities with human voices, which offers compelling evidence for cross-species vocal processing in the human auditory system. Overall, the study presents intellectually stimulating hypotheses and demonstrates methodological originality. However, the current findings are not yet solid enough to fully support the proposed claims, and the presentation could be enhanced for clarity and impact.
Reviewer #3 (Public review):
Summary:
Ceravolo et al. employed functional magnetic resonance imaging (fMRI) to examine how the temporal voice areas (TVA) in the human brain respond to vocalizations from different nonhuman primate species. Their findings reveal that the human TVA is not only responsible for human vocalizations but also exhibits sensitivity to the vocalizations of other primates, particularly chimpanzee vocalizations sharing acoustic similarities with human voices, which offers compelling evidence for cross-species vocal processing in the human auditory system. Overall, the study presents intellectually stimulating hypotheses and demonstrates methodological originality. However, the current findings are not yet solid enough to fully support the proposed claims, and the presentation could be enhanced for clarity and impact.
Strengths:
The study presents intellectually stimulating hypotheses and demonstrates methodological originality.
Weaknesses:
(1) The analysis of the fMRI data does not account for the participants' behavioral performance, specifically their reaction times (RTs) during the species categorization task.
(2) The figure organization/presentation requires significant revision to avoid confusion and redundancy.
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