Biology subjects

Gruber, T.

Publications and source records attributed to Gruber, T..

At least 19 recordsLinked to original sources

bioRxiv2026

Magel2 deficiency drives microglial synaptic engulfment and alters neuron-microglia interactions in Prader-Willi syndrome

Prader-Willi syndrome (PWS) is a neurodevelopmental disorder characterized by hypothalamic dysfunction, developmental delay, hyperphagia, and cognitive impairment, yet the cellular mechanisms underlying circuit abnormalities remain unclear. Here, we show that loss of the imprinted gene Magel2 remodels microglial state and function in a mouse model of PWS. Three-dimensional morphometric analysis of hypothalamic microglia revealed reduced structural complexity and contracted territorial domains, emerging early in development and largely independent of obesity. Single-nucleus RNA sequencing of hypothalamic brain tissue identified extensive transcriptional reprogramming involving immune signaling, cellular communication, ribosome function, synaptic organization, and protein translation, with stronger effects in females. Magel2 deficiency also increased microglia-neuron contacts and synaptic engulfment, accompanied by reduced synaptic marker density, suggesting aberrant refinement of hypothalamic circuits. Analyses of human post-mortem hypothalamic tissue from individuals with PWS confirmed microglial structural alterations and increased complement engagement. Ligand-receptor inference further revealed reorganization of microglia-centered communication networks, including altered adhesion, trophic, and immune signaling consistent with enhanced phagocytic states. Together, these findings identify microglial remodeling and increased synaptic engagement as central features of Magel2 deficiency, implicate microglia in hypothalamic circuit dysfunction in PWS, and highlight excessive synaptic pruning as a novel dysfunctional mechanism of PWS.

neuroscience↗

bioRxiv2026

Midbrain Tet1 dosage defines inter-individual binge-eating susceptibility

Binge-eating disorder (BED) is the most common eating disorder worldwide and carries life-altering comorbidities. While genetic and environmental risk factors have been identified, the mechanisms that determine inter-individual susceptibility to BED remain largely unknown. Here, we demonstrate that developmental dosage of the DNA hydroxymethylase Tet1 defines stable inter-individual differences in binge-eating susceptibility. In mice, midbrain dopaminergic neurons of the ventral tegmental area (VTADA) are essential for the induction of addictive binge-eating behavior, express high levels of Tet1, and undergo rapid and widespread DNA hydroxymethylation remodeling upon experimental binge eating. Strikingly, Tet1 haploinsufficiency creates pronounced inter-individual variation in binge-eating susceptibility even among genetically identical mice, which we trace to reduced connectivity between the prelimbic medial prefrontal cortex (mPFCPL) and the VTA. Chemogenetic inhibition of mPFCPL[->]VTA projections reduces binge-eating susceptibility, whereas EGR1-guided re-activation of TET1 in VTA dopaminergic neurons restores susceptibility, supporting a causal role for this axis. Importantly, TET1 promoter methylation in patients associates with binge-eating behavior and reward-circuit function, suggesting conservation of this regulatory network in humans. Collectively, these findings identify Tet1 dosage as a novel regulator of binge-eating susceptibility and provide a mechanistic basis for how inter-individual differences in behavior are established.

neuroscience↗

bioRxiv2026

Wild chimpanzees in Bugoma Forest, Uganda follow the Ugandan feeding ecology etiquette but exhibit cultural singularities: a case for the cultural junction hypothesis

Chimpanzees, amongst other primates, are characterized by the large variability of habitats they can be found in as well as a large behavioral, sometimes cultural diversity. Such observations have launched a decades-long debate on the roots of behavioral diversity, stressing the need to document this behavioral variability in context, such as by connecting closely related populations through localized analyses. This study presents the first comprehensive description of feeding ecology from the Mwera South chimpanzee (Pan troglodytes schweinfurthii) community in the Bugoma Central Forest Reserve, in Uganda, establishing a valuable baseline for this previously unstudied population and providing a comparative perspective on the populations of Western Uganda and Eastern Democratic Republic of Congo. By employing multiple methodological approaches, including direct observation and fecal analysis, we describe dietary composition, seasonal patterns, and environmental influences on feeding behavior. Characterizing the feeding ecology of this previously unstudied population is critical for examining how ecological factors might influence how feeding patterns evolve depending on resource availability or chimpanzee behavior, in particular by favoring analyses at the regional level. In addition, we can better evaluate to what extent behavioral differences between chimpanzee communities stem from ecological constraints and/or cultural transmission pathways. Our findings suggest that the Bugoma chimpanzees seat at the location of a historic cultural junction, opening a large array of questions about historic movements and cultural diffusion in Eastern chimpanzees.

animal behavior and cognition↗

bioRxiv2025

Variation in cultural attitude, knowledge and individual motivational factors impact engagement and tool use in a field experiment in wild chimpanzees

Cultural traditions shape how animals approach and solve problems. Previously, Ugandan chimpanzees (Pan trogodytes schweinfurthii), have engaged with the honey-trap experiment, an apparatus designed to mimic a beehive and provide ecological opportunities for tool use, relying on their cultural knowledge. Here, we presented chimpanzees from the Mwera South community, a newly habituated community in Bugoma Forest, with variations of the honey-trap experiment and compared their engagement to other Ugandan chimpanzee communities to investigate various aspects of cultural behaviour in animals. First, we wanted to test whether communities varied in cultural attitude towards a given food, and whether this attitude correlated with particular instrumental components of their cultural knowledge. Second, we were interested in analyzing individual variation across individuals within the same culture. Comparing individuals from Bugomas Mwera South (N=15), Budongos Sonso (N=34), and Kibales Kanyawara (N=14) communities, we found that the latter both exhibited higher engagement with the honey-trap, and a dedicated instrumental method, stick use, to obtain the honey. In contrast, Sonso and Mwera South chimpanzees appeared similar in lacking a cultural attitude towards honey, with no attached tool technique overall. Nevertheless, there were also strong inter-individual differences. Notably, some Mwera South chimpanzees displayed undescribed behavioural flexibility, using a range of tool behaviours including both stick and leaf tool use --a pattern never before documented in over a decade of honey-trap experiments. These results demonstrate that cultural attitudes toward resources constitute an additional layer to culture in addition to instrumental knowledge, and that the latter two coexist with individual motivational traits in influencing the realization of cultural behaviour.

animal behavior and cognition↗

bioRxiv2025

Sensitivity of the human temporal voice areas to nonhuman primate vocalizations

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.

neuroscience↗

bioRxiv2024

Mechanism of SHP2 activation by bis-Tyr-phosphorylated Gab1

The non-receptor tyrosine phosphatase SHP2 (PTPN11) is a regulator of diverse cellular functions including mitogenic activation and cell migration. SHP2 consists of two tandem SH2 domains followed by the catalytic domain, and is autoinhibited by the N-terminal SH2 domain that blocks access to the active site. Mutations that influence auto-inhibition have been implicated in cancer and other diseases, and allosteric inhibitors have been developed that stabilise the inactive state. The mechanism of SHP2 activation remains unclear, however. Here, we show that the intrinsically disordered bis-phosphorylated SHP2-activating peptide pY627pY659-Gab1 binds to both SH2 domains, undergoing a partial disorder-to-order transition in the process. In addition to eliciting changes in SH2 domain dynamics, the peptide reorganises their relative orientations to provide a new SH2-SH2 interface. Our data suggest an active conformation for SHP2 that is also applicable to the hematopoietic cell-specific SHP1 (PTPN6), shedding light on the activation mechanism of both enzymes and paving the way for the development of novel compounds that modulate SHP2 activity.

biochemistry↗

bioRxiv2024

Old age variably impacts chimpanzee engagement and efficiency in stone tool use

We know vanishingly little about how long-lived apes experience senescence in the wild, particularly with respect to their foraging behaviors, which are essential for survival. Some wild apes use tools during foraging and, given the additional cognitive and physical challenges presented by tool use, we predict that such behaviors are at a heightened risk of senescence. However, until the present, longitudinal analysis of the effects of progressive aging on wild ape tool-use behaviors has not been possible due to a lack of available data. In response to this research gap, we sampled data from a longitudinal video archive that contained footage of wild chimpanzees engaging in one of their most complex forms of tool use - the cracking of hard-shelled nuts with hammers and anvil stones, termed nut cracking - at an outdoor laboratory at Bossou, Guinea. By sampling data over a 17-year period, we describe how the extent to which wild chimpanzees engage in - and efficiently perform - nut cracking changes between the ages of approximately 39-44 to 56-61 years of age. Over this extended sampling period, chimpanzees began attending experimental nut cracking sites less frequently than younger individuals. Several elderly chimpanzees exhibited reductions in efficiency across multiple components of nut cracking, including taking more time to select stone tools prior to use, and taking longer to crack open nuts and consume the associated pieces of kernel. Two chimpanzees also began using less streamlined behavioral sequences to crack nuts, including a greater number of actions (such as more numerous strikes of the hammer stone). Most notably, we report interindividual variability in the extent to which elderly chimpanzees tool-use behaviors changed during our sample period - ranging from small to profound reductions in tool engagement and efficiency - as well as differences in the specific aspects of nut cracking behaviors that changed for each individual as they aged. We discuss the possible causes of these changes with reference to research into senescence in captive primates, and provide future directions for research of primate aging in both captive and wild settings.

animal behavior and cognition↗

bioRxiv2024

Nonadjacent Dependencies and Syntactic Structure of Chimpanzee Action During a Natural Tool-Use Task

The hierarchical organization of sequential behaviour, and the ability to compensate for nonadjacent sequential dependencies, are fundamental and interrelated abilities supporting complex human behaviours, including language and tool use. To understand how the cognition underlying these structural properties of human behaviour evolved, we can gain valuable insight from studying the sequential behaviours of nonhuman animals. Among the behaviours of nonhuman apes, tool use has been hypothesised to be a domain of behaviour which likely involves hierarchical organization. However thus far, evidence supporting this hypothesis comes from methodologies which have been criticised in their objectivity. Additionally, the extent to which nonadjacent dependencies appear in primate action sequences during tool use has not been formally investigated. We used estimations of mutual information (MI) - a measure of dependency strength between sequence elements - to evaluate both the extent to which wild chimpanzees produce nonadjacent dependencies during a naturalistic tool-use task (nut cracking), as well as how sequences of actions are organized during tool use. Half of adult chimpanzees produce nonadjacent dependencies at significantly greater sequential distances than comparable, nonhierarchical Markov models, including when repeated actions had been accounted for. Additionally, for the majority of chimpanzees, MI decay with increasing sequential distance included a power-law relationship, which is a key indicator that most chimpanzees draw upon forms of hierarchical structuring when organizing behaviours during tool use. Our analysis offered the greatest support for a system of organization which involved the production of short subroutines of actions (2-8 actions), which are hierarchically arranged into sequences - a finding which is consistent with previous qualitative descriptions of ape tool-use behaviours. Interindividual variability was detected within our analysis in both the distance dependencies were detected, and the most likely structuring mechanism for sequential action organization. We discuss these results in light of possible interindividual variation, in addition to methodological considerations for applications of MI estimations to sequential behaviours. Moreover, we discuss our main findings alongside hypotheses for the coevolution of complex syntax in language and tool-action across hominin evolutionary history.

animal behavior and cognition↗

bioRxiv2023

Self-assembly of Grb2 meshworks revealed by Grb2-Gab1497-528 complex structure

The ubiquitously expressed adaptor protein Growth factor receptor bound protein 2 (Grb2) plays an essential role in signal transduction by binding to activated receptor tyrosine kinases through its SH2 domain and to downstream effectors via its N- and C-terminal SH3 domains (nSH3, cSH3). Here we present the first structure of ligand-bound full length Grb2. The crystal structure of Grb2 in complex with a bidentate nSH3-cSH3-binding peptide, derived from the multi-site docking protein Grb2- associated binder-1 (Gab1), provides molecular insight into effector recognition by Grb2 and reveals the assembly of a two-dimensional meshwork, consisting of multimeric filament-like Grb2 chains linked to each other by the bivalent bound Gab1497-528 peptide. Dominant contacts between Grb2 molecules in the multimer are provided by an intermolecular SH2/cSH3 domain interface that is also present in the closed dimer of ligand-free Grb2. We further show that Grb2 is able to self-assemble to form phase-separated condensates in solution. The Grb2 SH2 domain phosphotyrosine binding site is freely accessible in the multimeric assembly, and phase separation is fostered by addition of Gab1497- 528, as expected from the crystal structure. Multimeric assembly is also observed using a Grb2 SH2- cSH3 didomain construct, and suppressed using a Grb2 Tyr60Glu mutant, a mimic of the in vivo phosphorylated Tyr160 central to the SH2/cSH3 interface, demonstrating that an intact SH2/cSH3 interface is needed for Grb2 assembly in solution.

biochemistry↗

bioRxiv2023

Model-based frontal cortex analysis reveals origins of human non-verbal communication

The ability to process verbal language seems unique to humans and relies not only on semantics but on other forms of communication such as affective vocalisations, that we share with other primate species--particularly great apes (Hominidae). To better understand these processes at the behavioural and brain level, we asked human participants to categorize vocalizations of four primate species including human, great apes (chimpanzee and bonobo), and monkey (rhesus macaque) during MRI acquisition. Classification was above chance level for all species but bonobo vocalizations. Imaging analyses were computed using a participant-specific, trial-by-trial fitted probability categorization value in a model-based style of data analysis. Model-based analyses revealed the implication of the bilateral orbitofrontal cortex and inferior frontal gyrus pars triangularis (IFGtri) respectively correlating and anti-correlating with the fitted probability of accurate species classification. Further conjunction analyses revealed enhanced activity in a sub-area of the left IFGtri specifically for the accurate classification of chimpanzee calls compared to human voices. Our data therefore reveal distinct frontal mechanisms that shed light on how the human brain evolved to process non-verbal language. Author contributionsCD and LC were involved in every steps of the study including experimental design, programming, data acquisition, data analysis and redaction of the first draft of the manuscript and subsequent editing. EP helped design the model-based MRI analyses and interpret the results. TG and DG were involved in the experimental design and study planification. All authors wrote and edited the manuscript.

neuroscience↗

bioRxiv2023

Identification of two β-cell subtypes by 7 independent criteria

Despite the recent explosion in surveys of cell-type heterogeneity, the mechanisms that specify and stabilize highly related cell subtypes remain poorly understood. Here, focusing initially on exploring quantitative histone mark heterogeneity, we identify two major sub-types of pancreatic {beta}-cells ({beta}HI and {beta}LO). {beta}HI and {beta}LO cells differ in their size, morphology, cytosolic and nuclear ultrastructure, transcriptional output, epigenomes, cell surface marker, and function. Importantly, {beta}HI and {beta}LO cells can be FACS separated live into CD24+ ({beta}HI) and CD24- ({beta}LO) fractions. From an epigenetic viewpoint, {beta}HI-cells exhibit [~]4-fold higher levels of H3K27me3, more compacted chromatin, and distinct chromatin organization that associates with a specific pattern of transcriptional output. Functionally, {beta}HI cells have increased mitochondrial mass, activity, and insulin secretion both in vivo and ex vivo. Critically, Eed and Jmjd3 loss-of-function studies demonstrate that H3K27me3 dosage is a significant regulator of {beta}HI / {beta}LO cell ratio in vivo, yielding some of the first-ever specific models of {beta}-cell sub-type distortion. {beta}HI and {beta}LO sub-types are conserved in humans with {beta}HI-cells enriched in human Type-2 diabetes. These data identify two novel and fundamentally distinct {beta}-cell subtypes and identify epigenetic dosage as a novel regulator of {beta}-cell subtype specification and heterogeneity. HighlightsO_LIQuantitative H3K27me3 heterogeneity reveals 2 common {beta}-cell subtypes C_LIO_LI{beta}HI and {beta}LO cells are stably distinct by 7 independent sets of parameters C_LIO_LIH3K27me3 dosage controls {beta}HI / {beta}LO ratio in vivo C_LIO_LI{beta}HI and {beta}LO cells are conserved in humans and enriched in Type-2 diabetes C_LI

cell biology↗

bioRxiv2022

Habitual ground nesting in the Bugoma Forest chimpanzees (Pan troglodytes schweinfurthii), Uganda.

We report the presence of habitual ground nesting in a newly studied East African chimpanzee (Pan troglodytes schweinfurthii) population in the Bugoma Central Forest Reserve, Uganda. Across a 2-year period we encountered 891 night-nests, 189 of which were classified as ground nests, a rate of [~]21%. We find no preliminary evidence of socio-ecological factors that would promote its use and highlight local factors, such as high incidence of forest disturbance due to poaching and logging, which appear to make its use disadvantageous. While further study is required to establish whether this behaviour meets the strict criteria for non-human animal culture, we support the argument that the wider use of population and group-specific behavioural repertoires in flagship species, such as chimpanzees, offers a tool to promote the urgent conservation action needed to protect threatened ecosystems, including the Bugoma forest.

ecology↗

bioRxiv2022

Two-Dimensional-Dwell-Time Analysis of Ion Channel Gating using High Performance Computing Clusters

The power of single-channel patch-clamp recordings is widely acknowledged among ion channel enthusiasts. The method allows observing the action of a single protein complex in real time and hence the deduction of the underlying conformational changes in the ion channel protein. Commonly, recordings are modeled using hidden Markov chains, connecting open and closed states in the experimental data with protein conformations. The rates between states denote transition probabilities that, for instance, could be modified by membrane voltage or ligand binding. Preferably, the time resolution of recordings should be in the range of microseconds or below, potentially bridging Molecular Dynamic simulations and experimental patch-clamp data. Modeling algorithms have to deal with limited recording bandwidth and a very noisy background. It was previously shown that the fit of 2-Dimensional-Dwell-Time histograms (2D-fit) with simulations is very robust in that regard. Errors introduced by the low-pass filter or noise cancel out to a certain degree when comparing experimental and simulated data. In addition, the topology of models, that is, the chain of open and closed states could be inferred from 2D-histograms. However, the 2D-fit was never applied to its full potential. The reason was the extremely time-consuming and unreliable fitting process, due to the stochastic variability in the simulations. We have now solved both issues by introducing a Message Passing Interface (MPI) allowing massive parallel computing on a High Performance Computing (HPC) cluster and obtaining ensemble solutions. With the ensembles, we have optimized the fit algorithm and demonstrated how important the ranked solutions are for difficult tasks related to a noisy background, fast gating events beyond the corner frequency of the low-pass filter and topology estimation of the underlying Markov model. The fit can reliably extract events down to a signal-to-noise ratio of one and rates up to ten times higher than the filter frequency. It is even possible to identify equivalent Markov topologies. Finally, we have shown that, by combining the objective function of the 2D-fit with the deviation of the current amplitude distributions automatic determination of the current level of the conducting state is possible. It is even possible to infer the level with an apparent current reduction due to the application of the low-pass filter. Making use of an HPC cluster, the power of 2D-Dwell-Time analysis can be used to its fullest, allowing extraction of the matching Markov model from a time series with minor input of the experimenter. Additionally, we add the benefit of estimating the reliability of the results by generating ensemble solutions.

physiology↗

bioRxiv2022

Coupling of oxytocin and cholecystokinin pathways in the hypothalamus is required for gut-to-brain homeostatic feeding control

Oxytocin-expressing paraventricular hypothalamic neurons (PVNOT neurons) integrate afferent signals from the gut including cholecystokinin (CCK) to adjust whole-body energy homeostasis. However, the molecular underpinnings by which PVNOT neurons orchestrate gut-to-brain feeding control remain unclear. Here, we show that mice undergoing selective ablation of PVNOT neurons fail to reduce food intake in response to CCK and develop hyperphagic obesity on chow diet. Notably, exposing wildtype mice to a high-fat/high-sugar (HFHS) diet recapitulates this insensitivity towards CCK, which is linked to diet-induced transcriptional and electrophysiological aberrations specifically in PVNOT neurons. Restoring OT pathways in DIO mice via chemogenetics or polypharmacology sufficiently re-establishes CCKs anorexigenic effects. Lastly, by single-cell profiling, we identify a specialized PVNOT neuronal subpopulation with increased {kappa}-opioid signaling under HFHS diet, which restrains their CCK-evoked activation. In sum, we here document a novel (patho)mechanism by which PVNOT signaling uncouples a gut-brain satiation pathway under obesogenic conditions.

neuroscience↗

bioRxiv2022

Cerebral activity in monkeys Papio anubis during the perception of conspecific and heterospecific agonistic vocalizations: A functional Near Infrared Spectroscopy study

Are conspecific emotional vocalizations special? Although often investigated in non-human primates using functional magnetic resonance imaging or positron emission tomography, it remains unclear whether the listening of conspecific vocal emotions leads to similar or different cerebral activations when compared to heterospecific calls (i.e. expressed by another primate species). Using a neuroimaging technique rarely employed in monkeys so far, functional Near Infrared Spectroscopy (fNIRS), the present study investigated cortical temporal activities during exposure to both conspecific and heterospecific calls in three female adult baboons (Papio anubis). The three subjects were lightly anesthetized and passively exposed to agonistic baboon and chimpanzee (Pan troglodytes) vocalizations, as well as energy matched white noises in order to control for this low-level acoustic feature. Despite inter-individual variabilities, permutation test analyses on the extracted OxyHemoglobin signal revealed for two subjects out of three significant differences between the passive listening of baboon versus chimpanzee stimuli. Additionally, in one subject, a modulation of the left temporal cortex activity was found for the perception of baboon calls contrasted to chimpanzee vocalizations as well as for the passive listening of baboon white noises compared to chimpanzee ones. Although the lack of generalization of those findings in all three subjects prevents us to drawn any conclusion and that more subjects would be needed, the hypothesis that baboons cortical temporal regions may be more sensitive to the processing of conspecific sounds compared to heterospecific stimuli is not excluded. Our study highlights that fNIRS may be a promising alternative to further investigate the auditory mechanisms at play in the right and left baboons temporal cortices for the processing of emotional vocalizations.

neuroscience↗

bioRxiv2022

Hypercaloric diet triggers transient molecular rearrangements of astrocytes selectively in the arcuate nucleus

Hypothalamic astrocytes are particularly affected by energy-dense food consumption. How the anatomical location of these glial cells and their spatial molecular distribution in the arcuate nucleus of the hypothalamus (ARC) determine the cellular response to a high caloric diet remains unclear. In this study, we investigated their distinctive molecular responses following the exposure to a high-fat high-sugar (HFHS) diet, specifically in the ARC. Using RNA sequencing and proteomics, we showed that astrocytes have a distinct transcriptomic and proteomic profile dependent on their anatomical location, with a major proteomic reprogramming in hypothalamic astrocytes. By ARC single-cell sequencing, we observed that a HFHS diet dictates time- and cell-specific transcriptomic responses, revealing that astrocytes have the most distinct regulatory pattern compared to other cell types. Lastly, we topographically and molecularly characterized astrocytes expressing glial fibrillary acidic protein and/or aldehyde dehydrogenase 1 family member L1 in the ARC, of which the abundance was significantly increased, as well as the alteration in their spatial and molecular profiles, with a HFHS diet. Together, our results provide a detailed multi-omics view on the spatial and temporal changes of astrocytes particularly in the ARC during different time points of adaptation to a high caloric diet.

neuroscience↗

bioRxiv2022

Categorization and discrimination of human and non-human primate affective vocalizations: investigation of the frontal cortex activity through fNIRS.

Many species, including humans and non-human primates, react differently to threatening or pleasant situations. Because of its adaptiveness, recognizing affective signals is likely to be reflected in a capability of modern humans to recognize other closely related species call content. However, at both behavioural and neural levels, only few studies have used a comparative approach to understand affective decoding processes in humans, particularly with respect to affective vocalizations. Previous research in neuroscience about the recognition of human affective vocalizations has shown the critical involvement of temporal and frontal regions. In particular, frontal regions have been reported as crucial in the explicit decoding of vocal emotions especially in different task complexity such as discrimination or categorization. The aim of this study using functional Near Infrared Spectroscopy (fNIRS) was to specifically investigate the neural activity of the inferior frontal cortex pars triangularis (IFGtri) and the prefrontal cortex (PFC) underlying categorization (A versus B) and discrimination (A versus non-A) mechanisms of positive and negative affects in human, great apes (chimpanzee and bonobo), and monkey (rhesus macaque) vocalizations. We also analysed participants behavioural responses and correlated them with the recorded frontal activations. While performing the tasks, fNIRS data revealed a clear distinction between the two frontal regions, with a general positive activation of IFGtri compared to a decrease of PFC activity. We also found a modulation of IFGtri and PFC activations depending on both the species considered and on task complexity; with generally more activity in the IFGtri during discrimination compared to categorization, and a more intense decrease of the PFC in categorization compared to discrimination. Behaviourally, participants recognized almost all affective cues in all species vocalizations at above chance levels in the discrimination task (except for threatening bonobo calls). For categorization, they mostly correctly identified at levels significantly above chance affective contents in human and great ape vocalizations but not in macaque calls. Overall, these findings support the hypothesis of a pre-human origin of affective recognition processing inherited from our common ancestor with other great apes and processed in the frontal cortex. Our results also highlight behavioural differences related to task complexity, i.e. between categorization and discrimination processes, and the differential involvement of the PFC and the IFGtri, which seems necessary to explicitly decode affects in all primate vocalizations.

neuroscience↗

bioRxiv2022

Humans recognize affective cues in primate vocalizations: Acoustic and phylogenetic perspectives

Humans are adept in extracting affective information from the vocalisations of not only humans but also other animals. Current research has mainly focused on phylogenetic proximity to explain such cross-species emotion recognition abilities. However, because research protocols are inconsistent across studies, it remains unclear whether human recognition of vocal affective cues of other species is due to cross-taxa similarities between acoustic parameters, the phylogenetic distances between species, or a combination of both. To address this, we first analysed acoustic variation in 96 affective vocalizations, including agonistic and affiliative contexts, of humans and three other primate species - rhesus macaques, chimpanzees and bonobos - the latter two being equally phylogenetically distant from humans. Using Mahalanobis distances, we found that chimpanzee vocalizations were acoustically closer to those of humans than to those of bonobos, confirming a potential derived vocal evolution in the bonobo lineage. Second, we investigated whether 68 human participants recognized the affective basis of vocalisations through tasks by asking them to categorize ( A vs B) or discriminate ( A vs non-A) vocalisations based on their affective content. Results showed that participants could reliably categorize and discriminate most of the affective vocal cues expressed by other primates, except threat calls by bonobos and macaques. Overall, participants showed greatest accuracy in detecting chimpanzee vocalizations; but not bonobo vocalizations, which provides support for both the phylogenetic proximity and acoustic similarity hypotheses. Our results highlight for the first time the importance of both phylogenetic and acoustic parameter level explanations in cross-species affective perception, drawing a more complex picture to explain our natural understanding of animal signals.

animal behavior and cognition↗