Vocalizations play an important role in the daily life of primates and likely form the basis of h... more Vocalizations play an important role in the daily life of primates and likely form the basis of human language. Functional imaging studies have demonstrated that listening to language or reading activates a left-lateralized fronto-temporal language network in human participants. Here we acquired whole-brain ultrahigh field (9.4 Tesla) fMRI in awake marmosets (Callithrix jacchus) and demonstrate that these highly vocal small New World primates possess a similar fronto-temporal network, including subcortical regions, that is activated by the presentation of conspecific vocalizations. The findings suggest that the human language network has evolved from an ancestral vocalization network that predates the separation of New and Old World primates.
The observation of others’ actions activates a network of temporal, parietal and premotor/prefron... more The observation of others’ actions activates a network of temporal, parietal and premotor/prefrontal areas in macaque monkeys and humans. This action-observation network (AON) has been shown to play important roles in understanding the actions of others, learning by imitation, and social cognition in both species. It is unclear whether a similar network exists in New World primates, which separated from Old Word Primates ∼ 35 million years ago. Here we used ultra-high field fMRI at 9.4T in awake common marmosets (Callithrix jacchus) while they watched videos depicting the upper-limb of conspecifics performing goal-directed (grasping food) or non-goal-directed actions. We found that the observation of goal-directed actions, compared to non-goal directed ones, activated a temporo-parieto-frontal network, including areas 6 and 45 in premotor and prefrontal cortices, areas PGa-IPa, FST and the TE complex in occipito-temporal region and areas V6A, MIP, LIP and PG in the occipito-parietal...
The observation of others’ actions activates a network of temporal, parietal and premotor/prefron... more The observation of others’ actions activates a network of temporal, parietal and premotor/prefrontal areas in macaque monkeys and humans. This action-observation network (AON) has been shown to play important roles in social action monitoring, learning by imitation, and social cognition in both species. It is unclear whether a similar network exists in New-World primates, which separated from Old-Word primates ~35 million years ago. Here we used ultra-high field fMRI at 9.4 T in awake common marmosets (Callithrix jacchus) while they watched videos depicting goal-directed (grasping food) or non-goal-directed actions. The observation of goal-directed actions activates a temporo-parieto-frontal network, including areas 6 and 45 in premotor/prefrontal cortices, areas PGa-IPa, FST and TE in occipito-temporal region and areas V6A, MIP, LIP and PG in the occipito-parietal cortex. These results show overlap with the humans and macaques’ AON, demonstrating the existence of an evolutionarily ...
Theory of Mind (ToM) refers to the ability to ascribe mental states to other individuals. This pr... more Theory of Mind (ToM) refers to the ability to ascribe mental states to other individuals. This process is so strong that it extends even to the attribution of mental states to animations depicting interacting simple geometric shapes, such as in the Frith-Happé animations in which two triangles move either purposelessly (Random condition), or as if one triangle is reacting to the other triangle’s mental state (ToM condition). Currently, there is no evidence that nonhuman primates attribute mental states to moving abstract shapes. Here we investigated whether highly social marmosets (Callithrix jacchus) process ToM and Random Frith-Happé animations differently. Our results show that marmosets and humans (1) follow more closely one of the triangles during the observation of ToM compared to Random animations, and (2) activate large and comparable brain networks when viewing ToM compared to Random animations. These findings indicate that marmosets, like humans, process ToM animations dif...
The correct identification of facial expressions is critical for understanding the intention of o... more The correct identification of facial expressions is critical for understanding the intention of others during social communication in the daily life of all primates. Here we used ultra-high-field fMRI at 9.4 T to investigate the neural network activated by facial expressions in awake New World common marmosets from both male and female sex, and to determine the effect of facial motions on this network. We further explored how the face-patch network is involved in the processing of facial expressions. Our results show that dynamic and static facial expressions activate face patches in temporal and frontal areas (O, PV, PD, MD, AD, and PL) as well as in the amygdala, with stronger responses for negative faces, also associated with an increase of the respiration rates of the monkey. Processing of dynamic facial expressions involves an extended network recruiting additional regions not known to be part of the face-processing network, suggesting that face motions may facilitate the recognition of facial expressions. We report for the first time in New World marmosets that the perception and identification of changeable facial expressions, vital for social communication, recruit face-selective brain patches also involved in face detection processing and are associated with an increase of arousal.SIGNIFICANCE STATEMENTRecent research in humans and nonhuman primates has highlighted the importance to correctly recognize and process facial expressions to understand others' emotions in social interactions. The current study focuses on the fMRI responses of emotional facial expressions in the common marmoset (Callithrix jacchus), a New World primate species sharing several similarities of social behavior with humans. Our results reveal that temporal and frontal face patches are involved in both basic face detection and facial expression processing. The specific recruitment of these patches for negative faces associated with an increase of the arousal level show that marmosets process facial expressions of their congener, vital for social communication.
Understanding the default-mode network (DMN) in the common marmoset (Callithrix jacchus) has been... more Understanding the default-mode network (DMN) in the common marmoset (Callithrix jacchus) has been challenging due to inconsistencies with human and marmoset DMNs. By analyzing task-negative activation in fMRI studies, we identified medial prefrontal cortical areas, rostral auditory areas, entorhinal cortex, posterior cingulate cortex area 31, hippocampus, hypothalamus, and basomedial amygdala as marmoset DMN components. Notable, medial and posterior parietal areas that were previously hypothesized to be part of the DMN were activated during visual task blocks. Seed analysis using resting-state fMRI showed strong connectivity between task-negative areas, and tracer data supported a structural network aligning with this functional DMN. These findings challenge previous definition of the marmoset DMN and reconcile many inconsistencies with the DMNs observed in humans, macaque monkeys, and even rodents. Overall, these results highlight the marmoset as a powerful model for DMN research, ...
SummaryPrimate communication relies on multimodal cues, such as vision and audition, to facilitat... more SummaryPrimate communication relies on multimodal cues, such as vision and audition, to facilitate the exchange of intentions, enable social interactions, avoid predators, and foster group cohesion during daily activities. Understanding the integration of facial and vocal signals is pivotal to comprehend social interaction. In this study, we acquired whole-brain ultra-high field (9.4T) fMRI data from awake marmosets (Callithrix jacchus) to explore brain responses to unimodal and combined facial and vocal stimuli. Our findings reveal that the multisensory condition not only intensified activations in the occipito-temporal ‘face patches’ and auditory ‘voice patches’ but also engaged a more extensive network that included additional parietal, prefrontal and cingulate areas, compared to the summed responses of the unimodal conditions. By uncovering the neural network underlying multisensory audiovisual integration in marmosets, this study highlights the efficiency and adaptability of th...
Accumulating evidence indicates that the peripersonal space (PPS) constitutes a privileged area f... more Accumulating evidence indicates that the peripersonal space (PPS) constitutes a privileged area for efficient processing of proximal stimuli, allowing to flexibly adapt our behavior both to the physical and social environment. Whether and how behavioral and physiological signatures of PPS relate to each other in emotional contexts remains, though, elusive. Here, we addressed this question by having participants to discriminate male from female faces depicting different emotions (happiness, anger or neutral) and presented at different distances (50 cm-300 cm) while we measured the reaction time and accuracy of their responses, as well as pupillary diameter, heart rate and heart rate variability. Results showed facilitation of participants' performances (i.e., faster response time) when faces were presented close compared to far from the participants, even when controlling for retinal size across distances. These behavioral effects were accompanied by significant modulation of participants' physiological indexes when faces were presented in PPS. Interestingly, both PPS representation and physiological signals were affected by features of the seen faces such as the emotional valence, its sex and the participants' sex, revealing the profound impact of social context onto the autonomic state and behavior within PPS. Together, these findings suggest that both external and internal signals contribute in shaping PPS representation.
The chocolate plumage color in chickens is due to a sex-linked recessive mutation, choc, which di... more The chocolate plumage color in chickens is due to a sex-linked recessive mutation, choc, which dilutes eumelanin pigmentation. Because TYRP1 is sex-linked in chickens, and TYRP1 mutations determine brown coat color in mammals, TYRP1 appeared as the obvious candidate gene for the choc mutation. By combining gene mapping with gene capture, a complete association was identified between the chocolate phenotype and a missense mutation leading to a His214Asn change in the ZnA zinc-binding domain of the protein. A diagnostic test confirmed complete association by screening 428 non-chocolate chickens of various origins. This is the first TYRP1 mutation described in the chicken. Electron microscopy analysis showed that melanosomes were more numerous in feather follicles of chocolate chickens but exhibited an abnormal structure characterized by a granular content and an irregular shape. A similar altered morphology was observed on melanosomes of another TYRP1 mutant in birds, the roux mutation of the quail. This article is protected by copyright. All rights reserved.
A critical aspect of neuroscience is to establish whether and how brain networks evolved across p... more A critical aspect of neuroscience is to establish whether and how brain networks evolved across primates. To date, most comparative studies have used resting-state functional Magnetic Resonance Imaging (rs-fMRI) in anaesthetized non-human primates and in awake humans. However, anaesthesia strongly affects rs-fMRI signals. The present study investigated the impact of the awareness state (anaesthesia vs. awake) within the same group of macaque monkeys on the rs-fMRI functional connectivity (FC) organization of a well characterized network in the human brain, the cingulo-frontal lateral network. Results in awake macaques revealed a similar FC pattern to that previously uncovered in the human brain. Rostral seeds in the cingulate sulcus exhibited stronger correlation strength with rostral compared to caudal lateral frontal cortical areas while caudal seeds in the cingulate sulcus displayed stronger correlation strength with caudal compared to anterior lateral frontal cortical areas. Cri...
Vocalizations play an important role in the daily life of primates and likely form the basis of h... more Vocalizations play an important role in the daily life of primates and likely form the basis of human language. Functional imaging studies have demonstrated that listening to language or reading activates a left-lateralized fronto-temporal language network in human participants. Here we acquired whole-brain ultrahigh field (9.4 Tesla) fMRI in awake marmosets (Callithrix jacchus) and demonstrate that these highly vocal small New World primates possess a similar fronto-temporal network, including subcortical regions, that is activated by the presentation of conspecific vocalizations. The findings suggest that the human language network has evolved from an ancestral vocalization network that predates the separation of New and Old World primates.
The observation of others’ actions activates a network of temporal, parietal and premotor/prefron... more The observation of others’ actions activates a network of temporal, parietal and premotor/prefrontal areas in macaque monkeys and humans. This action-observation network (AON) has been shown to play important roles in understanding the actions of others, learning by imitation, and social cognition in both species. It is unclear whether a similar network exists in New World primates, which separated from Old Word Primates ∼ 35 million years ago. Here we used ultra-high field fMRI at 9.4T in awake common marmosets (Callithrix jacchus) while they watched videos depicting the upper-limb of conspecifics performing goal-directed (grasping food) or non-goal-directed actions. We found that the observation of goal-directed actions, compared to non-goal directed ones, activated a temporo-parieto-frontal network, including areas 6 and 45 in premotor and prefrontal cortices, areas PGa-IPa, FST and the TE complex in occipito-temporal region and areas V6A, MIP, LIP and PG in the occipito-parietal...
The observation of others’ actions activates a network of temporal, parietal and premotor/prefron... more The observation of others’ actions activates a network of temporal, parietal and premotor/prefrontal areas in macaque monkeys and humans. This action-observation network (AON) has been shown to play important roles in social action monitoring, learning by imitation, and social cognition in both species. It is unclear whether a similar network exists in New-World primates, which separated from Old-Word primates ~35 million years ago. Here we used ultra-high field fMRI at 9.4 T in awake common marmosets (Callithrix jacchus) while they watched videos depicting goal-directed (grasping food) or non-goal-directed actions. The observation of goal-directed actions activates a temporo-parieto-frontal network, including areas 6 and 45 in premotor/prefrontal cortices, areas PGa-IPa, FST and TE in occipito-temporal region and areas V6A, MIP, LIP and PG in the occipito-parietal cortex. These results show overlap with the humans and macaques’ AON, demonstrating the existence of an evolutionarily ...
Theory of Mind (ToM) refers to the ability to ascribe mental states to other individuals. This pr... more Theory of Mind (ToM) refers to the ability to ascribe mental states to other individuals. This process is so strong that it extends even to the attribution of mental states to animations depicting interacting simple geometric shapes, such as in the Frith-Happé animations in which two triangles move either purposelessly (Random condition), or as if one triangle is reacting to the other triangle’s mental state (ToM condition). Currently, there is no evidence that nonhuman primates attribute mental states to moving abstract shapes. Here we investigated whether highly social marmosets (Callithrix jacchus) process ToM and Random Frith-Happé animations differently. Our results show that marmosets and humans (1) follow more closely one of the triangles during the observation of ToM compared to Random animations, and (2) activate large and comparable brain networks when viewing ToM compared to Random animations. These findings indicate that marmosets, like humans, process ToM animations dif...
The correct identification of facial expressions is critical for understanding the intention of o... more The correct identification of facial expressions is critical for understanding the intention of others during social communication in the daily life of all primates. Here we used ultra-high-field fMRI at 9.4 T to investigate the neural network activated by facial expressions in awake New World common marmosets from both male and female sex, and to determine the effect of facial motions on this network. We further explored how the face-patch network is involved in the processing of facial expressions. Our results show that dynamic and static facial expressions activate face patches in temporal and frontal areas (O, PV, PD, MD, AD, and PL) as well as in the amygdala, with stronger responses for negative faces, also associated with an increase of the respiration rates of the monkey. Processing of dynamic facial expressions involves an extended network recruiting additional regions not known to be part of the face-processing network, suggesting that face motions may facilitate the recognition of facial expressions. We report for the first time in New World marmosets that the perception and identification of changeable facial expressions, vital for social communication, recruit face-selective brain patches also involved in face detection processing and are associated with an increase of arousal.SIGNIFICANCE STATEMENTRecent research in humans and nonhuman primates has highlighted the importance to correctly recognize and process facial expressions to understand others' emotions in social interactions. The current study focuses on the fMRI responses of emotional facial expressions in the common marmoset (Callithrix jacchus), a New World primate species sharing several similarities of social behavior with humans. Our results reveal that temporal and frontal face patches are involved in both basic face detection and facial expression processing. The specific recruitment of these patches for negative faces associated with an increase of the arousal level show that marmosets process facial expressions of their congener, vital for social communication.
Understanding the default-mode network (DMN) in the common marmoset (Callithrix jacchus) has been... more Understanding the default-mode network (DMN) in the common marmoset (Callithrix jacchus) has been challenging due to inconsistencies with human and marmoset DMNs. By analyzing task-negative activation in fMRI studies, we identified medial prefrontal cortical areas, rostral auditory areas, entorhinal cortex, posterior cingulate cortex area 31, hippocampus, hypothalamus, and basomedial amygdala as marmoset DMN components. Notable, medial and posterior parietal areas that were previously hypothesized to be part of the DMN were activated during visual task blocks. Seed analysis using resting-state fMRI showed strong connectivity between task-negative areas, and tracer data supported a structural network aligning with this functional DMN. These findings challenge previous definition of the marmoset DMN and reconcile many inconsistencies with the DMNs observed in humans, macaque monkeys, and even rodents. Overall, these results highlight the marmoset as a powerful model for DMN research, ...
SummaryPrimate communication relies on multimodal cues, such as vision and audition, to facilitat... more SummaryPrimate communication relies on multimodal cues, such as vision and audition, to facilitate the exchange of intentions, enable social interactions, avoid predators, and foster group cohesion during daily activities. Understanding the integration of facial and vocal signals is pivotal to comprehend social interaction. In this study, we acquired whole-brain ultra-high field (9.4T) fMRI data from awake marmosets (Callithrix jacchus) to explore brain responses to unimodal and combined facial and vocal stimuli. Our findings reveal that the multisensory condition not only intensified activations in the occipito-temporal ‘face patches’ and auditory ‘voice patches’ but also engaged a more extensive network that included additional parietal, prefrontal and cingulate areas, compared to the summed responses of the unimodal conditions. By uncovering the neural network underlying multisensory audiovisual integration in marmosets, this study highlights the efficiency and adaptability of th...
Accumulating evidence indicates that the peripersonal space (PPS) constitutes a privileged area f... more Accumulating evidence indicates that the peripersonal space (PPS) constitutes a privileged area for efficient processing of proximal stimuli, allowing to flexibly adapt our behavior both to the physical and social environment. Whether and how behavioral and physiological signatures of PPS relate to each other in emotional contexts remains, though, elusive. Here, we addressed this question by having participants to discriminate male from female faces depicting different emotions (happiness, anger or neutral) and presented at different distances (50 cm-300 cm) while we measured the reaction time and accuracy of their responses, as well as pupillary diameter, heart rate and heart rate variability. Results showed facilitation of participants' performances (i.e., faster response time) when faces were presented close compared to far from the participants, even when controlling for retinal size across distances. These behavioral effects were accompanied by significant modulation of participants' physiological indexes when faces were presented in PPS. Interestingly, both PPS representation and physiological signals were affected by features of the seen faces such as the emotional valence, its sex and the participants' sex, revealing the profound impact of social context onto the autonomic state and behavior within PPS. Together, these findings suggest that both external and internal signals contribute in shaping PPS representation.
The chocolate plumage color in chickens is due to a sex-linked recessive mutation, choc, which di... more The chocolate plumage color in chickens is due to a sex-linked recessive mutation, choc, which dilutes eumelanin pigmentation. Because TYRP1 is sex-linked in chickens, and TYRP1 mutations determine brown coat color in mammals, TYRP1 appeared as the obvious candidate gene for the choc mutation. By combining gene mapping with gene capture, a complete association was identified between the chocolate phenotype and a missense mutation leading to a His214Asn change in the ZnA zinc-binding domain of the protein. A diagnostic test confirmed complete association by screening 428 non-chocolate chickens of various origins. This is the first TYRP1 mutation described in the chicken. Electron microscopy analysis showed that melanosomes were more numerous in feather follicles of chocolate chickens but exhibited an abnormal structure characterized by a granular content and an irregular shape. A similar altered morphology was observed on melanosomes of another TYRP1 mutant in birds, the roux mutation of the quail. This article is protected by copyright. All rights reserved.
A critical aspect of neuroscience is to establish whether and how brain networks evolved across p... more A critical aspect of neuroscience is to establish whether and how brain networks evolved across primates. To date, most comparative studies have used resting-state functional Magnetic Resonance Imaging (rs-fMRI) in anaesthetized non-human primates and in awake humans. However, anaesthesia strongly affects rs-fMRI signals. The present study investigated the impact of the awareness state (anaesthesia vs. awake) within the same group of macaque monkeys on the rs-fMRI functional connectivity (FC) organization of a well characterized network in the human brain, the cingulo-frontal lateral network. Results in awake macaques revealed a similar FC pattern to that previously uncovered in the human brain. Rostral seeds in the cingulate sulcus exhibited stronger correlation strength with rostral compared to caudal lateral frontal cortical areas while caudal seeds in the cingulate sulcus displayed stronger correlation strength with caudal compared to anterior lateral frontal cortical areas. Cri...
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