Biology subjects

Everling, S.

Publications and source records attributed to Everling, S..

At least 37 records · Page 2Linked to original sources

bioRxiv2023

Laminar Dynamics of Target Selection in the Posterior Parietal Cortex of the Common Marmoset

The lateral intraparietal area (LIP) plays a crucial role in target selection and attention in primates, but the laminar microcircuitry of this region is largely unknown. To address this, we used ultra-high density laminar electrophysiology with Neuropixels probes to record neural activity in the posterior parietal cortex (PPC) of two adult marmosets while they performed a simple visual target selection task. Our results reveal neural correlates of visual target selection in the marmoset, similar to those observed in macaques and humans, with distinct timing and profiles of activity across cell types and cortical layers. Notably, a greater proportion of neurons exhibited stimulus related activity in superficial layers whereas a greater proportion of infragranular neurons exhibited significant post-saccadic activity. Stimulus-related activity was first observed in granular layer putative interneurons, whereas target discrimination activity emerged first in supragranular layers putative pyramidal neurons, supporting a canonical laminar circuit underlying visual target selection in marmoset PPC. These findings provide novel insights into the neural basis of visual attention and target selection in primates.

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bioRxiv2023

Mapping of Facial and Vocal Processing in Common Marmosets with ultra-high field fMRI

Primate 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 the marmoset brain in processing facial and vocal social signals, providing significant insights into primate social communication.

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bioRxiv2023

Effects of ketamine on frontoparietal interactions during working memory in macaque monkeys

Schizophrenia is known as a syndrome of dysconnection among brain regions. As a model for this syndrome, low doses of N-methyl-D-aspartate (NMDA) receptor antagonists, such as ketamine, produce schizophrenia-like symptoms and cognitive deficits in healthy humans and animals. One of such deficits is impaired working memory, a process that engages an extended network of both frontal and parietal areas. While ketamine is known to disrupt working memory by altering both spiking and oscillatory activities in the lateral prefrontal cortex (lPFC), it remains unknown whether NMDA receptor antagonists also produce frontoparietal dysconnection during working memory processes. Here, we simultaneously recorded both single unit activities and local field potentials from lPFC and posterior parietal cortex (PPC) in macaque monkeys during a rule-based working memory task. Like previous work in the lPFC alone, we found that ketamine compromised delay-period rule coding in single neurons and reduced low-frequency oscillations in the PPC. Furthermore, ketamine reduced task-related connectivity in both fronto-parietal and parieto-frontal directions. Consistent with this, ketamine also weakened interareal coherence between spiking and low-frequency oscillatory activities. Our findings demonstrate the utility of acute NMDA receptor antagonist in simulating a syndrome of dysconnection and support this model in its potential for the exploration of novel treatment strategies for schizophrenia.

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bioRxiv2023

A vocalization-processing network in marmosets

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.

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bioRxiv2023

Gaze patterns and brain activations in humans and marmosets in the Frith-Happe; theory-of-mind animation task

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-Happe animations in which two triangles move either purposelessly (Random condition), or as if one triangle is reacting to the other triangles 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-Happe 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 differently from Random animations.

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bioRxiv2022

Perception of dynamic facial expressions activates a cortico-subcortico-cerebellar network in marmosets

The perception and identification of faces and facial emotional expressions are critical for social communication in the daily life of all primates. Here, we investigated the neural network activated by dynamic facial expressions in awake New World common marmosets with ultra-high field fMRI at 9.4T. Our results show that dynamic facial expressions activate several areas along the occipitotemporal axis (V2/V3, V4/TEO, FST, caudal TE, rostral TE, TPO), frontal cortex (areas 45/47, 13, 8a and orbital cortex), amygdala, motion-sensitive areas, premotor area, and in the posterior lobe of the cerebellum. Negative faces increased the monkeys respiration rates and elicited stronger responses along the occipitotemporal cortical axis, in the amygdala and in the hypothalamus. This cortico-subcortico-cerebellar network may play an important role in the perception of behaviorally relevant facial expressions that are vital for social communication in marmosets. Significance StatementRecent research has highlighted the importance of emotional content of faces in social communication in humans and non-human primates. The current study focuses on the neural responses to dynamic emotional facial expressions in the common marmoset (Callithrix jacchus), a New World primate species sharing several similarities of social behavior with humans. Using ultra-high-field fMRI, we show that negative facial expressions activate a cortico-subcortico-cerebellar network and, critically, negative faces increase the level of arousal of marmosets, possibly relayed through a modulation of the activity in the autonomic nervous system via stress-integrative brain centres in the hypothalamus. Our results reveal the existence of specific neural and physiological responses to negative emotional faces suggesting that behaviorally relevant facial expressions are vital for social communication in New World marmosets.

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bioRxiv2022

An action-observation network in the common marmoset identified by ultra-high field fMRI

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 cortex. These results show remarkable overlap with the AON observed in humans and macaques. These results demonstrate the existence of an evolutionarily conserved AON that likely predates the separation of Old and New World primates.

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bioRxiv2022

Delay-related activity in marmoset prefrontal cortex

Persistent delay-period activity in prefrontal cortex (PFC) has long been regarded as a neural signature of working memory (WM). Electrophysiological investigations in macaque PFC have provided much insight into WM mechanisms, however a barrier to understanding is the fact that a portion of PFC lies buried within the principal sulcus in this species and is inaccessible for laminar electrophysiology or optical imaging. The relatively lissencephalic cortex of the New World common marmoset (Callithrix jacchus) circumvents such limitations. It remains unknown however, whether marmoset PFC neurons exhibit persistent activity. Here, we addressed this gap by conducting wireless electrophysiological recordings in PFC of marmosets performing a delayed-match-to-location task on a home cage-based touchscreen system. As in macaques, marmoset PFC neurons exhibited sample, delay, and response-related activity that was directionally tuned and linked to correct task performance. Models constructed from population activity consistently and accurately predicted stimulus location throughout the delay period, supporting a framework of delay activity in which mnemonic representations are relatively stable in time. Taken together, our findings support the existence of common neural mechanisms underlying WM performance in PFC of macaques and marmosets, and thus validate the marmoset as a suitable model animal for investigating the microcircuitry underlying WM.

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bioRxiv2021

Functional organization of frontoparietal cortex in the marmoset investigated with awake resting-state fMRI

Frontoparietal networks contribute to complex cognitive functions in humans and macaques such as working memory, attention, task-switching, response suppression, grasping, reaching, and eye movement control. However, little is known about the organization of frontoparietal networks in the New World common marmoset monkey (Callithrix jacchus) which is now widely recognized as a powerful nonhuman primate experimental animal. In this study, we employed hierarchical clustering of interareal BOLD signals to investigate the hypothesis that the organization of the frontoparietal cortex in the marmoset follows the organizational principles of the macaque frontoparietal system. We found that the posterior part of the lateral frontal cortex (premotor regions) was functionally connected to the anterior parietal areas while more anterior frontal regions (frontal eye field (FEF)) were connected to more posterior parietal areas (the area around lateral intraparietal area (LIP)). These overarching patterns of inter-areal organization are consistent with a recent macaque study. These findings demonstrate parallel frontoparietal processing streams in marmosets and support the functional homologies of FEF-LIP and premotor-anterior parietal pathways between marmoset and macaque. Significant StatementFrontoparietal networks contribute to many cognitive functions in humans and macaques, but little is known about the organization of frontoparietal networks in the New World common marmoset monkey. Here, we investigated the hypothesis that the organization of the frontoparietal cortex in the marmoset follows the organizational principles of the macaque frontoparietal system. These frontoparietal connection showed overarching pattern of interareal organization consistent with Old world monkeys. These findings demonstrate parallel frontoparietal processing streams in marmosets.

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bioRxiv2021

Ketamine disrupts gaze patterns during face viewing in the common marmoset

Faces are stimuli of critical importance for primates. The common marmoset (Callithrix jacchus) is a promising model for investigations of face processing, as this species possesses oculomotor and face processing networks resembling those of macaques and humans. Face processing is often disrupted in neuropsychiatric conditions such as schizophrenia (SZ) and thus it is important to recapitulate underlying circuitry dysfunction preclinically. The N-Methyl-D-aspartate (NMDA) non-competitive antagonist ketamine has been used extensively to model the cognitive symptoms of SZ. Here, we investigated the effects of a subanesthetic dose of ketamine on oculomotor behaviour in marmosets during face viewing. Four marmosets received systemic ketamine or saline injections while viewing phase-scrambled or intact videos of conspecifics faces. To evaluate effects of ketamine on scan paths during face viewing, we identified regions of interest in each face video, and classified locations of saccade onsets and landing positions within these areas. A preference for the snout over eye regions was observed following ketamine administration. In addition, regions in which saccades landed could be significantly predicted by saccade onset region in the saline but not the ketamine condition. No significant drug effects were observed for phase-scrambled videos. Effects on saccade control were limited to a reduction in saccade amplitudes during viewing of scrambled videos. Thus, ketamine induced a significant disruption of scan paths during viewing of conspecific faces but limited effects on saccade motor control. These findings support the use of ketamine in marmosets for investigating changes in neural circuits underlying social cognition in neuropsychiatric disorders.

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bioRxiv2021

Interspecies activation correlations reveal functional correspondences between marmoset and human brain areas

The common marmoset has enormous promise as a nonhuman primate model of human brain functions. While resting-state functional magnetic resonance imaging (fMRI) has provided evidence for a similar organization of marmoset and human cortices, the technique cannot be used to map the functional correspondences of brain regions between species. This limitation can be overcome by movie-driven fMRI (md-fMRI), which has become a popular tool for non-invasively mapping the neural patterns generated by rich and naturalistic stimulation. Here, we used md-fMRI in marmosets and humans to identify whole-brain functional correspondences between the two primate species. In particular, we describe functional correlates for the well-known human face, body, and scene patches in marmosets. We find that these networks have a similar organization in both species, suggesting a largely conserved organization of higher-order visual areas between New World marmoset monkeys and humans. However, while face patches in humans and marmosets were activated by marmoset faces, only human face patches responded to the faces of other animals. Together, the results demonstrate that md-fMRI is a powerful tool for interspecies functional mapping and characterization of higher-order visual functions.

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bioRxiv2021

Simultaneous functional MRI of socially interacting marmosets

Social cognition is a dynamic process that requires the perception and integration of a complex set of idiosyncratic features between interacting conspecifics. Here we present a method for simultaneously measuring the whole-brain activation of two socially interacting marmoset monkeys using functional magnetic resonance imaging. MRI hardware (a radiofrequency coil and peripheral devices) and image-processing pipelines were developed to assess brain responses to socialization, both on an intra-brain and inter-brain level. Notably, brain-activation maps acquired during constant interaction demonstrated neuronal synchrony between marmosets in regions of the brain responsible for processing social interaction. This method enables a wide range of possibilities for studying social function and dysfunction in a non-human primate model, including using transgenic models of neuropsychiatric disorders.

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bioRxiv2020

Whole brain mapping of somatosensory responses in awake marmosets investigated with ultra-high field fMRI

The common marmoset (Callithrix jacchus) is a small-bodied New World primate that is becoming an important model to study brain functions. Despite several studies exploring the somatosensory system of marmosets, all results have come from anesthetized animals using invasive techniques and post-mortem analyses. Here we demonstrate the feasibility for getting high-quality and reproduceable sensorimotor mapping in awake marmosets with functional magnetic resonance imaging (fMRI). We acquired fMRI sequences in four animals while they received tactile stimulation (via air-puffs), delivered to the face, arm or leg. We found that the body representation progressed medially from the leg to the face in areas 3a, 3b, 1/2, and from caudal to rostral sites in areas S2 and PV. SI and SII exhibited a body representation in their functional connectivity pattern within the posterior and midcingulate and the thalamus. Interestingly, we also found a somatotopic body representation in two subcortical areas: the thalamus and, for the first time, in the putamen. These maps have similar organizations as those previously found in Old World macaque monkeys and humans, suggesting that these subcortical somatotopic organizations were already established before Old and New World primates diverged. Our results show the first whole brain mapping of somatosensory responses acquired in a non-invasive way in awake marmosets. Significant statementHere we used somatosensory stimulation combined with functional magnetic resonance imaging to map whole brain activation in awake marmosets. We used light tactile stimulation, consisting of air-puffs, delivered on the face, arm or leg. We found a topographic body representation in primary (SI) and secondary (SII) somatosensory regions, thalamus and putamen. We also revealed the existence of a body representation organization within the thalamus and the cingulate cortex by computing functional connectivity maps from seeds defined in SI/SII for face, arm and leg using resting-state fMRI data. This non-invasive approach will be essential for chronic studies by guiding invasive recording and manipulation techniques.

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bioRxiv2020

Cortico-subcortical functional connectivity profiles of resting-state networks in marmosets and humans

Understanding the similarity of cortico-subcortical networks topologies between humans and nonhuman primate species is critical to study the origin of network alternations underlying human neurological and neuropsychiatric diseases. The New World common marmoset (Callithrix jacchus) has become popular as a non-human primate model for human brain function. Most marmoset connectomic research, however, has exclusively focused on cortical areas, with connectivity to subcortical networks less extensively explored. In this study, we aimed to first isolate patterns of subcortical connectivity with cortical resting-state networks (RSNs) in awake marmosets using resting-state functional magnetic resonance imaging (RS-fMRI), then to compare these networks to those in humans using connectivity fingerprinting. While we could match several marmoset and human RSNs based on their functional fingerprints, we also found a few striking differences, for example strong functional connectivity of the default mode network with the superior colliculus in marmosets that was much weaker in humans. Together, these findings demonstrate that many of the core cortico-subcortical networks in humans are also present in marmosets, but that small, potentially functionally relevant differences exist.

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bioRxiv2020

Structural alterations in the macaque frontoparietal white matter network after recovery from prefrontal cortex lesions

Unilateral damage to the frontoparietal network typically impairs saccade target selection within the contralesional visual hemifield. Severity of deficits and the degree of recovery have been associated with widespread network dysfunction, yet it is not clear how these behavioural and functional changes relate with the underlying structural white matter pathways. Here, we investigated whether recovery after unilateral prefrontal cortex (PFC) lesions was associated with structural white matter remodeling in the distributed frontoparietal network. Diffusion-weighted MRI was acquired in four macaque monkeys before the lesions and at 2-4 months post-lesion, after recovery of deficits in saccade selection of contralesional targets. Probabilistic tractography was used to reconstruct inter- and intra-hemispheric frontoparietal fiber tracts: bilateral superior longitudinal fasciculus (SLF) and transcallosal fibers connecting bilateral PFC or bilateral posterior parietal cortex (PPC). After behavioural recovery, tract-specific fractional anisotropy in contralesional SLF and transcallosal PPC increased after small lesions and decreased after larger lesions compared to pre-lesion. These findings indicate that remote fiber tracts may provide optimal compensation after small PFC lesions. However, larger lesions may have induced widespread structural damage and hindered compensatory remodeling in the structural frontoparietal network.

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bioRxiv2020

Face selective patches in marmoset frontal cortex

Primates have evolved the ability transmit important social information through facial expression. In humans and macaque monkeys, socially relevant face processing is accomplished via a distributed cortical and subcortical functional network that includes specialized patches in anterior cingulate cortex and lateral prefrontal cortex, regions usually associated with high-level cognition. It is unclear whether a similar network exists in New World primates, who diverged ~35 million years from Old World primates and have a less elaborated frontal cortex. The common marmoset (Callithrix jacchus) is a small New World primate that is ideally placed to address this question given the complex social repertoire inherent to this species (e.g., observational social learning; imitation; cooperative antiphonal calling). Here, we investigated the existence of a putative high-level face processing network in marmosets by employing ultra-high field (9.4 Tesla) task-based functional MRI (fMRI). We demonstrated that, like Old World primates, marmosets show differential activation in anterior cingulate cortex and lateral prefrontal cortex while they view socially relevant videos of marmoset faces. We corroborate the locations of these frontal regions by demonstrating both functional (via resting-state fMRI) and structural (via cellular-level tracing) connectivity between these regions and temporal lobe face patches. Given the evolutionary separation between macaques and marmosets, our results suggest this frontal network specialized for social face processing predates the separation between Platyrrhini and Catarrhine. These results give further credence to the marmoset as a viable preclinical modelling species for studying human social disorders.

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bioRxiv2019

Dynamic reconfiguration, fragmentation and integration of whole-brain modular structure across depths of unconsciousness

General anesthetics are routinely used to induce unconsciousness, and much is known about their effects on receptor function and single neuron activity. Much less is known about how these local effects are manifest at the whole-brain level, nor how they influence network dynamics, especially past the point of induced unconsciousness. Using resting-state functional magnetic resonance imaging (fMRI) with nonhuman primates, we investigated the dose-dependent effects of anesthesia on whole-brain temporal modular structure, following loss of consciousness. We found that higher isoflurane dose was associated with an increase in both the number and isolation of whole-brain modules, as well as an increase in the uncoordinated movement of brain regions between those modules. Conversely, we found that higher dose was associated with a decrease in the cohesive movement of brain regions between modules, as well as a decrease in the proportion of modules in which brain regions participated. Moreover, higher dose was associated with a decrease in the overall integrity of networks derived from the temporal modules, with the exception of a single, sensory-motor network. Together, these findings suggest that anaesthesia-induced unconsciousness results from the hierarchical fragmentation of dynamic whole-brain network structure, leading to the discoordination of temporal interactions between cortical modules.

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bioRxiv2019

Visual looming and receding networks in awake marmosets investigated with fMRI

An object that is looming toward a subject or receding away contains important information for determining if this object is dangerous, beneficial or harmless to them. This information (motion, direction, identity, time-to-collision, size, velocity) is analyzed by the brain in order to execute the appropriate behavioral responses depending on the context: fleeing, freezing, grasping, eating, exploring. In the current study, we performed ultra-high-field functional MRI (fMRI) in awake marmosets to explore the patterns of brain activation elicited by visual stimuli looming toward or receding away from the monkey. We found that looming and receding visual stimuli both activate a large cortical network in frontal, parietal, temporal and occipital cortex in areas involved in the analysis of motion, shape, identity and features of the objects. Looming stimuli strongly activated a network composed of the pulvinar, superior colliculus, prefrontal cortex and temporal cortical areas. This may underlie the existence of an alert network that processes the visual stimuli looming toward their peripersonal space by extracting the crucial information brought by the stimulus and evaluating its potential consequences to the observer. We hypothesize that this network is involved in the planning of protective behaviors (e.g. fleeing or freezing) and in emotional reaction (e.g. anxiety, fear). These findings support the view that this network is preserved through evolution and that the marmoset is a viable model to study visual and multisensory processes by using fMRI to guide further invasive recordings and/or pharmacological manipulations.\n\nSignificant statementAn object that is looming toward a subject or receding away contains important information for determining if this object is dangerous, beneficial or harmless to them. Here, we identified the functional network in non-human primates that was activated by visual stimuli looming toward or away from the animals using ultra-high-field functional magnetic resonance imaging. Our findings show that large cortical activations are elicited by both looming and receding visual conditions. However, some activations were specific to the looming condition, suggesting that the integration of cues in the looming direction rely on strong connections between cortical and subcortical areas, which allows primates to react properly for protecting themselves against a potential threat.

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