The anterior cingulate cortex (ACC) is known to play a crucial role in the fast adaptations of behavior based on immediate reward values. What is less certain is whether the ACC is also involved in long-term adaptations to situations with uncertain outcomes. To study this issue, we placed macaque monkeys in a probabilistic context in which the appropriate strategy to maximize reward was to identify the stimulus with the highest reward value (optimal stimulus). Only knowledge of the theoretical average reward value associated with this stimulus--referred to as 'the task value'--was available. Remarkably, in each trial, ACC pre-reward activity correlated with the task value. Importantly, this neuronal activity was observed prior to the discovery of the optimal stimulus. We hypothesize that the received rewards and the task value, constructed a priori through learning, are used to guide behavior and identify the optimal stimulus. We tested this hypothesis by muscimol deactivation of the ACC. As predicted, this inactivation impaired the search for the optimal stimulus. We propose that ACC participates in long-term adaptation of voluntary reward-based behaviors by encoding general task values and received rewards.

SummaryNon-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 that have the necessary facilities and capabilities. The PRIMatE Data Exchange (PRIME-DE) addresses this challenge by aggregating independently acquired non-human primate magnetic resonance imaging (MRI) datasets and openly sharing them via the International Neuroimaging Data-sharing Initiative (INDI). Here, we present the rationale, design, and procedures for the PRIME-DE consortium, as well as the initial release, consisting of 25 independent data collections aggregated across 22 sites (total = 217 non-human primates). We also outline the unique pitfalls and challenges that should be considered in the analysis of non-human primate MRI datasets, including providing automated quality assessment of the contributed datasets.

Learning abilities depend on detection and exploitation of errors. In primates, this function involves the anterior cingulate cortex. However, whether anterior cingulate error-related activity indicates occurrence of inappropriate responses or results from other computations is debated. Here we have tested whether reward-related parameters modulate error-related activity of anterior cingulate neurons. Recordings in monkeys performing stimulus-reward associations and preliminary data obtained with a problem-solving task revealed major properties of error-related unit activity: (i) their amplitude varies with the amount of predicted reward or the proximity to reward delivery; (ii) they appear both after execution and performance errors; (iii) they do not indicate which error occurred or which correction to make; and (iv), importantly, the activity of these neurons also increases following an external signal indicating the necessity to shift response. Hence, we conclude that anterior cingulate 'error' activity might represent a negative deviation from a predicted goal, and does not only reflect error detection but signals events interrupting potentially rewarded actions.

A confusing picture of the functional organization of the dorsal premotor region of the human brain emerged when functional neuroimaging studies that either examined visuomotor hand conditional activity or attempted to localize the human frontal eye field reported activity increases at the same general location, namely the junction of the superior precentral sulcus with the superior frontal sulcus. The present functional magnetic resonance imaging study examined visuomotor hand conditional activity and the locus of the frontal eye field as defined by a standard task, on a subject-by-subject basis, to clarify their location and reveal relationships between the pattern of local morphology and functional activity. The results demonstrate that visuomotor hand conditional activity and the frontal eye field lie within distinct parts of the superior precentral sulcus, revealing an organization of the human premotor cortex consistent with that observed in experimental studies in the monkey.

In the monkey, 3 motor areas have been identified in the cortex occupying the banks of the cingulate sulcus (cgs): A rostral cingulate motor area and 2 caudal cingulate motor areas, 1 located in the dorsal bank and the other in the ventral bank of the sulcus. The homologs of these 3 cingulate motor areas in the human brain are poorly understood. The present functional magnetic resonance imaging study examined the anatomo-functional organization of the cingulate motor areas in the human brain. A subject by subject analysis revealed the existence of 3 motor areas along the cgs and these areas appear to be somatotopically organized. Importantly, these 3 motor areas relate to the specific morphological features of the cingulate/paracingulate cortex. These results demonstrate the location and organization of the 3 cingulate motor areas in the human brain and suggest a well-preserved organization of these motor areas from the monkey to the human brain.

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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 medial frontal cortex was assessed in Old World monkeys (macaque/baboon) and Hominoidea (chimpanzee/human). We show that both Hominoidea possess a paracingulate sulcus, which was previously thought to be unique to the human brain and linked to higher cognitive functions, such as mentalizing. Also, we show systematic sulcal morphological organization of the medial frontal cortex that can be traced from Old World monkeys to Hominoidea species, demonstrating an evolutionarily conserved organizational principle. These data provide a new framework to compare sulcal morphology, cytoarchitectonic areal distribution, connectivity, and function across the primate order, leading to clear predictions about how other primate brains might be anatomo-functionally organized.

The ventromedial prefrontal cortex (vmPFC), which comprises several distinct cytoarchitectonic areas, is a key brain region supporting decision-making processes, and it has been shown to be one of the main hubs of the Default Mode Network, a network classically activated during resting state. We here examined the interindividual variability in the vmPFC sulcal morphology in 57 humans (37 females) and demonstrated that the presence/absence of the inferior rostral sulcus and the subgenual intralimbic sulcus influences significantly the sulcal organization of this region. Furthermore, the sulcal organization influences the location of the vmPFC peak of the Default Mode Network, demonstrating that the location of functional activity can be affected by local sulcal patterns. These results are critical for the investigation of the function of the vmPFC and show that taking into account the sulcal variability might be essential to guide the interpretation of neuroimaging studies. SIGNIFICANCE STATEMENT The ventromedial prefrontal cortex (vmPFC) is one of the main hubs of the Default Mode Network and plays a central role in value coding and decision-making. The present study provides a complete description of the interindividual variability of anatomical morphology of this large portion of prefrontal cortex and its relation to functional organization. We have shown that two supplementary medial sulci predominantly determine the organization of the vmPFC, which in turn affects the location of the functional peak of activity in this region. Those results show that taking into account the variability in sulcal patterns might be essential to guide the interpretation of neuroimaging studies of the human brain and of the vmPFC in particular.