Emmanuel Procyk

French Institute of Health and Medical Research | Inserm · Stem Cell and Brain Research Institute

The functional and anatomical organization of the cingulate cortex across primate species is the subject of considerable and often confusing debate. The functions attributed to the midcingulate cortex (MCC) embrace, among others, feedback processing, pain, salience, action-reward association, premotor functions, and conflict monitoring. This multip...

Frontal beta oscillations are associated with top-down control mechanisms but also change over time during a task. It is unclear whether change over time represents another control function or a neural instantiation of vigilance decrements over time, the time-on-task effect. We investigated how frontal beta oscillations are modulated by cognitive c...

Curiosity and information seeking potently shapes our behaviour and are thought to rely on the frontal cortex. Yet, the frontal regions and neural dynamics that control the drive to check for information remain unknown. Here we trained monkeys in a task where they had the opportunity to gain information about the potential delivery of a large bonus...

The article ‘In vitro neurons learn and exhibit sentience when embodied in a simulated game-world’ by Kagan et al.1 triggered a wave of positive mainstream and scientific media coverage as well as a widespread negative reaction from the scientific community. Here, we discuss why this negative reaction is legitimate and must be taken seriously. We r...

Recent efforts to chart human brain growth across the lifespan using large-scale MRI data have provided reference standards for human brain development. However, similar models for nonhuman primate (NHP) growth are lacking. The rhesus macaque, a widely used NHP in translational neuroscience due to its similarities in brain anatomy, phylogenetics, c...

Recent efforts to chart human brain growth across the lifespan using large-scale MRI data have provided reference standards for human brain development. However, similar models for nonhuman primate (NHP) growth are lacking. The rhesus macaque, a widely used NHP in translational neuroscience due to its similarities in brain anatomy, phylogenetics, c...

The functional organization of the frontal lobe is a source of debate, focusing on broad functional subdivisions, large-scale networks, or local refined specificities. Multiple neurocognitive models have tried to explain how functional interactions between cingulate and lateral frontal regions contribute to decision making and cognitive control, bu...

Over the course of evolution, the amygdala (AMG) and medial frontal cortex (mPFC) network, involved in behavioral adaptation, underwent structural changes in the old-world monkey and human lineages. Yet, whether and how the functional organization of this network differs remains poorly understood. Using resting-state functional magnetic resonance i...

Deep brain stimulation of the subthalamic nucleus (STN) has become the gold standard surgical treatment for Parkinson’s disease and is being investigated for obsessive compulsive disorders. Even if the role of the STN in the behavior is well documented, its organization and especially its division into several functional territories is still debate...

The importance of studying the transient burst-like nature of beta- and gamma-band oscillations has become increasingly clear. This approach challenges accepted interpretations of oscillatory behavior and emphasizes the importance of examining phenomena at appropriate temporal scales, as opposed to trial averages. Diversity in the detailed temporal...

Identifying the evolutionary origins of human speech remains a topic of intense scientific interest. Here we describe a unique feature of adult human neuroanatomy compared to chimpanzees and other primates that may provide an explanation of changes that occurred to enable the capacity for speech. That feature is the Prefrontal extent of the Frontal...

Detailed neuroscientific data from macaque monkeys have been essential in advancing understanding of human frontal cortex function, particularly for regions of frontal cortex without homologs in other model species. However, precise transfer of this knowledge for direct use in human applications requires an understanding of monkey to hominid homolo...

Behavioral adaptations are triggered by different constraints given by rules, and are informed by outcomes, or motivational changes. Neural activity in multiple frontal areas is modulated during behavioral adaptations but the source of these modulations and the nature of the mechanisms involved are unclear. Here we tested how different variables re...

We apply Dynamic Causal Models to electrocorticogram recordings from two macaque monkeys performing a problem-solving task that engages working memory, and induces time-on-task effects. We thus provide a computational account of changes in effective connectivity within two regions of the fronto-parietal network, the dorsolateral prefrontal cortex a...

Research and developments based on nonhuman primate models have a specific place in biomedical sciences, and nonhuman primate species also have a specific place in the public opinion on the use of animal in research. While nonhuman primates are used in very limited number compared to other animal models, they are rightly the focus of deep ethical c...

Objectives In the human brain, the inferior frontal gyrus (IFG) is comprised of three morphological regions, which include the pars opercularis, pars triangularis, and pars orbitalis. These brains regions are implicated in a number of cognitive and linguistic functions, and the pars opercularis and pars triangularis of the language dominant hemisph...

Cortical dynamics are organized over multiple anatomical and temporal scales. The mechanistic origin of the temporal organization and its contribution to cognition remain unknown. Here we demonstrate the cause of this organization by studying a specific temporal signature (time constant and latency) of neural activity. In monkey frontal areas, reco...

In this paper, we provide a computational account of changes in synaptic connectivity within two regions of the fronto-parietal network, the dorsolateral prefrontal cortex and the pre-supplementary motor area, applying Dynamic Causal Models to electrocorticogram recordings from two macaque monkeys performing a problem-solving task that engages work...

Parkinson's disease (PD) evolves over an extended and variable period in humans; years prior to the onset of classical motor symptoms, sleep and biological rhythm disorders develop, significantly impacting the quality‐of‐life of patients. Circadian‐rhythm disorders are accompanied by mild cognitive deficits that progressively worsen with disease pr...

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 nonhuman primates and in awake humans. However, anaesthesia strongly affects rs-fMRI signals. The present study investiga...

Decisions made by mammals and birds are often temporally extended. They require planning and sampling of decision-relevant information. Our understanding of such decision-making remains in its infancy compared with simpler, forced-choice paradigms. However, recent advances in algorithms supporting planning and information search provide a lens thro...

A bstract 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 stud...

Electrophysiological markers of performance monitoring are thought to reflect functioning of dedicated neural networks and neuromodulatory systems. Whether and how these markers are altered in neurological diseases and whether they can reflect particular cognitive deficits remains to be confirmed. Here we first tested whether the frontal medial fee...

The ability to integrate information across time at multiple timescales is a vital element of adaptive behavior, because it provides the capacity to link events separated in time, extract useful information from previous events and actions, and to construct plans for behavior over time. Here we make the argument that this information integration ca...

Individual differences in sulcal variation within the anterior and mid-cingulate cortex of the human brain, particularly the presence or absence of a paracingulate sulcus (PCGS), are associated with various motor and cognitive processes. Recently, it has been reported that chimpanzees possess a PCGS, previously thought to be a unique feature of the...

Evolution, as we currently understand it, strikes a delicate balance between animals’ ancestral history and adaptations to their current niche. Similarities between species are generally considered inherited from a common ancestor whereas observed differences are considered as more recent evolution. Hence comparing species can provide insights into...

Cognitive deficits as well as disorders of sleep and biological rhythms constitute non-motor symptoms that significantly impact quality of life in Parkinson’s disease patients. Few studies have evaluated the impact of cell replacement therapy on such non-motor symptoms. Here we used a multidisciplinary approach to assess the therapeutic potential o...

Cognitive deficits as well as sleep and biological rhythm disorders constitute the non-motor symptoms that significantly impact quality of life in Parkinson’s disease. Few studies have evaluated the impact of cell replacement therapy on non-motor symptoms. Here we implement a multidisciplinary and multiparametric assessment of the therapeutic poten...

Cortical neural dynamics organizes over multiple anatomical and temporal scales. The mechanistic origin of the temporal organization and its contribution to cognition remain unknown. Here we demonstrate that a temporal signature (autocorrelogram time constant and latency) of neural activity enlightens this organization. In monkey frontal areas, rec...

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Evolution, as we currently understand it, strikes a delicate balance between animals' ancestral history and adaptations to their current niche. Similarities between species are generally considered inherited from a common ancestor whereas observed differences are considered more recent occurrences. Hence comparing species can provide insights into...

Nonhuman primate neuroimaging is on the cusp of a transformation, much in the same way its human counterpart was in 2010, when the Human Connectome Project was launched to accelerate progress. Inspired by an open data-sharing initiative, the global community recently met and, in this article, breaks through obstacles to define its ambitions.

In the primate brain, a set of areas in the ventrolateral frontal (VLF) cortex and the dorsomedial frontal (DMF) cortex appear to control vocalizations. The basic role of this network in the human brain and how it may have evolved to enable complex speech remain unknown. In the present functional neuroimaging study of the human brain, a multidomain...

The midcingulate cortex (MCC) is viewed as a central node within a large-scale system devoted to adjusting behavior in the face of changing environments. Whereas the role of the MCC in interfacing action and cognition is well established, its role in regulating the autonomic nervous system is poorly understood. Yet, adaptive reactions to novel or t...

Confidence judgments are self-assessments of the quality of one's own performance, and are a crucial aspect of metacognitive abilities. The underlying neurobiological mechanisms are poorly understood. One approach to understanding these mechanisms would be to take advantage of putative metacognitive abilities in non-human models. However, many disc...

Although the relative expansion of the frontal cortex in primate evolution is generally accepted, the nature of the human uniqueness, if any, and between-species anatomo-functional comparisons of the frontal areas remain controversial. To provide a novel interpretation of the evolution of primate brains, sulcal morphological variability of the medi...

The frontal cortical areas critical for human speech production, i.e. the ventrolateral frontal cortex (cytoarchitectonic areas 44 and 45; VLF) and the dorsomedial frontal cortex (DMF) comprising the mid-cingulate cortex (MCC) and the pre-supplementary motor area (preSMA), exist in non-human primates and are implicated in cognitive vocal control fu...

Although the relative expansion of the frontal cortex in primate evolution is generally accepted, the nature of the human uniqueness, if any, and between-species anatomo-functional comparisons of the frontal areas remain controversial. To provide a novel interpretation of the evolution of primate brains, sulcal morphological variability of the medi...

Non-human primate neuroimaging is a rapidly growing area of research that promises to transform and scale translational and cross-species comparative neuroscience. Unfortunately, the technological and methodological advances of the past two decades have outpaced the accrual of data, which is particularly challenging given the relatively few centers...

TE, echo time; TR, repetition time; PE, phase encoding; RO, read out direction; Reconstructed resolution (RR; mm) and image dimensions refer to the images after they have been reconstructed from the k-space data, the matrix size, and resolution used for the acquisition may differ. For these categories, RO, read out direction; PE, phase encoding dir...

FA, flip angle; TE, echo time; TR, repetition time; BW, bandwidth per pixel; ES, echo spacing; PA, parallel acquisition; PF, partial Fourier (half scan); PE, phase encoding direction; FS, fat suppression; SO, slice orientation; SA, slice acquisition order; Gap, gap between slices; RO, read out direction; Nacq, number of volumes collected; Ndisc, nu...

FA, flip angle; TE, echo time; TR, repetition time

FA, flip angle; TI, inversion time; TE, echo time; ES, echo spacing; BW, bandwidth per pixel; TR, repetition time; PA, parallel acquisition; PF, partial Fourier (half scan); SO, slice orientation; PE, phase encoding direction; RO, read out direction; SL, slice direction. Reconstructed resolution (RR; mm) and image dimensions (RID; px) refer to the...

The sulcal morphology of the human medial frontal cortex has received marked interest because of (1) its remarkable link with the functional organization of this region, and (2) observations that deviations from 'normal' sulcal morphological variability correlate with the prevalence of some psychiatric disorders, cognitive abilities, or personality...

Background: The advances in extracellular neural recording techniques result in big data volumes that necessitate fast, reliable, and automatic identification of statistically similar units. This study proposes a single framework yielding a compact set of probabilistic descriptors that characterise the firing patterns of a single unit. New method...

According to contemporary views, the lateral frontal cortex is organized along a rostro-caudal functional axis with increasingly complex cognitive/behavioral control implemented rostrally, and increasingly detailed motor control implemented caudally. Whether the medial frontal cortex follows the same organization remains to be elucidated. To addres...

Several premotor areas have been identified within primate cingulate cortex; however their function is yet to be uncovered. Recent brain imaging work in humans revealed a topographic anatomofunctional overlap between feedback processing during exploratory behaviors and the corresponding body fields in the rostral cingulate motor area (RCZa), sugges...

Accumulating evidence suggest that human behavior in trial-and-error learning tasks based on decisions between discrete actions may involve a combination of reinforcement learning (RL) and working-memory (WM). While the understanding of brain activity at stake in this type of tasks often involve the comparison with non-human primate neurophysiologi...

Accumulating evidence suggest that human behavior in trial-and-error learning tasks based on decisions between discrete actions may involve a combination of reinforcement learning (RL) and working-memory (WM). While the understanding of brain activity at stake in this type of tasks often involve the comparison with non-human primate neurophysiologi...

This work investigates the involvement of the Broca-MCC brain network in the cognitive control of vocal and orofacial responses. Within this network, Broca’s area was implicated in the conditional selection of vocal and orofacial responses but not manual responses. Within the MCC, the ’face’ representation of the rostral most cingulate motor area c...

In this work, we examine the functional connectivity of the three human cingulate motor areas, and their various motor representations, with the prefrontal and primary motor cortex.

Dopamine is thought to directly influence the neurophysiological mechanisms of both performance monitoring and cognitive control—two processes that are critically linked in the production of adapted behaviour. Changing dopamine levels are also thought to induce cognitive changes in several neurological and psychiatric conditions. But the working mo...

PST task example and ECoG implants. A. A sample time-course for a problem sequence in PST4. In the first problem, the monkey makes one incorrect response (INC) before finding the correct target (COR), and together these two trials are the SEA phase. The monkey then repeats this COR response three further times, completing the REP phase. An STC is t...

Equivalent of Fig 1D, but for reaction times (GO signal to lever release). As for response times, there is a significant difference for between high- and low-control trials, albeit one that is only marginally significant for Monkey R. (TIF)

Analysis of FRPs on search (SEA) trials, to assess the impact of outcome probability on effects. A. Difference waves in BL generated in the same way as Fig 2B, but here for the difference INC-CO1 (solid lines), and CO1-COR (dotted lines), where CO1 is the 1st correct feedback in each problem. B. Proportions of INC trials for the first three trials...

Binding of DAT as revealed by [11C]PE2I-BPND from PET imaging for the BL and then successive scans during the MPTP period. Each point represents the BPND measured for all voxels inside the Caudate, Putamen, and ACC cingulate ROIs as defined by Ballanger et al [57]. These data replicate the previous finding of Vezoli et al. [53] by showing an early...

ARRIVE Checklist completed for this study. (PDF)

Supplementary Figures 1-12

Primates display a remarkable ability to adapt to novel situations. Determining what is most pertinent in these situations is not always possible based only on the current sensory inputs, and often also depends on recent inputs and behavioral outputs that contribute to internal states. Thus, one can ask how cortical dynamics generate representation...

There are continuing uncertainties regarding whether performance monitoring recruits the anterior insula (aI) and/or the frontal operculum (fO). The proximity and morphological complexity of these two regions make proper identification and isolation of the loci of activation extremely difficult. The use of group averaging methods in human neuroimag...

Frontal cortical areas control behavioral adaptation to environmental rules. In particular, the dorsal Anterior Cingulate Cortex (dACC) is thought to signal the worth of updating the behavioral strategy to new evidence. Downstream areas would then process and store this signal to ultimately trigger the behavioral change when the opportunity arises...

Unexpected outcomes can reflect noise in the environment or a change in the current rules. We should ignore noise but shift strategy after rule changes. How we learn to do this is unclear, but one possibility is that it relies on learning to learn in uncertain environments. We propose that acquisition of latent task structure during learning to lea...

The frontal cortex controls behavioral adaptation in environments governed by complex rules. Many studies have established the relevance of firing rate modulation after informative events signaling whether and how to update the behavioral policy. However, whether the spatiotemporal features of these neuronal activities contribute to encoding immine...

This study seeks to characterize the neuronal mechanisms underlying voluntary decisions to check/verify. In order to describe and potentially decode decisions from brain signals we analyzed intracortical recordings from monkey prefrontal regions obtained during a cognitive task requiring self-initiated as well as cue-instructed decisions. Using loc...

Conference: XII International Conference on Cognitive Neuroscience (ICON-XII), Brisbane, Queensland, Australia, 27 Jul - 31 Jul, 2014. To explain the high level of flexibility of decision making in primates, theoretical models usually invoke reinforcement-based mechanisms, performance monitoring functions, and core neural features within frontal...