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An economic choice entails computing and comparing the values of individual offers. Offer values are represented in the orbitofrontal cortex (OFC)-an area that participates in value comparison-but it is unknown where offer values are computed in the first place. One possibility is that this computation takes place in OFC. Alternatively, offer values might be computed upstream of OFC. For choices between edible goods, a primary candidate is the gustatory region of the anterior insula (gustatory cortex, GC). Here we recorded from the GC of male rhesus monkeys choosing between different juice types. As a population, neurons in GC represented the flavor, the quantity, and the subjective value of the juice chosen by the animal. These variables were represented by distinct groups of cells and with different time courses. Specifically, chosen value signals emerged shortly after offer presentation, while neurons encoding the chosen juice and the chosen quantity peaked after juice delivery. Surprisingly, neurons in GC did not represent individual offer values in a systematic way. In a computational sense, the variables encoded in GC follow the process of value comparison. Thus our results argue against the hypothesis that offer values are computed in GC. At the same time, signals representing the subjective value of the expected reward indicate that responses in GC are not purely sensory. Thus neuronal responses in GC appear consummatory in nature.

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Primates interact with the world by exploring visual objects; they seek opportunities to view novel objects even when these have no extrinsic reward value. How the brain controls this novelty seeking is unknown. Here we show that novelty seeking in monkeys is regulated by the zona incerta (ZI). As monkeys made eye movements to familiar objects to trigger an opportunity to view novel objects, many ZI neurons were preferentially activated by predictions of novel objects before the gaze shift. Low-intensity ZI stimulation facilitated gaze shifts, whereas ZI inactivation reduced novelty seeking. ZI-dependent novelty seeking was not regulated by neurons in the lateral habenula or by many dopamine neurons in the substantia nigra, traditionally associated with reward seeking. But the anterior ventral medial temporal cortex, an area important for object vision and memory, was a prominent source of novelty predictions. These data uncover a functional pathway in the primate brain that regulates novelty seeking.

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Humans and animals can be strongly motivated to seek information to resolve uncertainty about rewards and punishments. In particular, despite its clinical and societal relevance, very little is known about information seeking about punishments. We show that attitudes toward information about punishments and rewards are distinct and separable at both behavioral and neuronal levels. We demonstrate the existence of prefrontal neuronal populations that anticipate opportunities to gain information in a relatively valence-specific manner, separately anticipating information about either punishments or rewards. These neurons are located in anatomically interconnected subregions of anterior cingulate cortex (ACC) and ventrolateral prefrontal cortex (vlPFC) in area 12o/47. Unlike ACC, vlPFC also contains a population of neurons that integrate attitudes toward both reward and punishment information, to encode the overall preference for information in a bivalent manner. This cortical network is well suited to mediate information seeking by integrating the desire to resolve uncertainty about multiple, distinct motivational outcomes.

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The brain mechanism for controlling continuous behavior in dynamic contexts must mediate action selection and learning across many timescales, responding differentially to the level of environmental uncertainty and volatility. In this review, we argue that a part of the frontal cortex known as the anterior cingulate cortex (ACC) is particularly well suited for this function. First, the ACC is interconnected with prefrontal, parietal, and subcortical regions involved in valuation and action selection. Second, the ACC integrates diverse, behaviorally relevant information across multiple timescales, producing output signals that temporally encapsulate decision and learning processes and encode high-dimensional information about the value and uncertainty of future outcomes and subsequent behaviors. Third, the ACC signals behaviorally relevant information flexibly, displaying the capacity to represent information about current and future states in a valence-, context-, task- and action-specific manner. Fourth, the ACC dynamically controls instrumental- and non-instrumental information seeking behaviors to resolve uncertainty about future outcomes. We review electrophysiological and circuit disruption studies in primates to develop this point, discuss its relationship to novel therapeutics for neuropsychiatric disorders in humans, and conclude by relating ongoing research in primates to studies of medial frontal cortical regions in rodents.

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Multiple lines of evidence link economic choices to the orbitofrontal cortex (OFC), but other brain regions may contribute to the computation and comparison of economic values. A particularly strong candidate is the basolateral amygdala (BLA). Amygdala lesions impair performance in reinforcer devaluation tasks, suggesting that the BLA contributes to value computation. Furthermore, previous studies of the BLA have found neuronal activity consistent with a value representation. Here, we recorded from the BLA of two male rhesus macaques choosing between different juices. Offered quantities varied from trial to trial, and relative values were inferred from choices. Approximately one-third of BLA cells were task-related. Our analyses revealed the presence of three groups of neurons encoding variables offer value, chosen value, and chosen juice In this respect, the BLA appeared similar to the OFC. The two areas differed for the proportion of neurons in each group, as the fraction of chosen value cells was significantly higher in the BLA. Importantly, the activity of these neurons reflected the subjective nature of value. Firing rates in the BLA were sustained throughout the trial and maximal after juice delivery. In contrast, firing rates in the OFC were phasic and maximal shortly after offer presentation. Our results suggest that the BLA supports economic choice and reward expectation.SIGNIFICANCE STATEMENT Economic choices rely on the orbitofrontal cortex (OFC), but other brain regions may contribute to this behavior. A strong candidate is the basolateral amygdala (BLA). Previous results are consistent with a neuronal representation of value, but the role of the BLA in economic decisions remains unclear. Here, we recorded from monkeys choosing between juices. Neurons in the BLA encoded three decision variables: offer value, chosen value, and chosen juice These variables were also identified in the OFC. The two areas differed in the proportion of cells encoding each variable and in the activation timing. In the OFC, firing rates peaked shortly after offer presentation; in the BLA, firing rates were sustained and peaked after juice delivery. These results suggest that the BLA supports choices and reward expectation.

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Over the past two decades, the insula has been described as the sensory "interoceptive cortex". As a consequence, human brain imaging studies have focused on its role in the sensory perception of emotions. However, evidence from neurophysiological studies in non-human primates have shown that the insula is also involved in generating emotional and communicative facial expressions. In particular, a recent study demonstrated that electrical stimulation of the mid-ventral sector of the insula evoked affiliative facial expressions. The present study aimed to describe the cortical connections of this "affiliative field". To this aim, we identified the region with electrical stimulation and injected neural tracers to label incoming and outgoing projections. Our results show that the insular field underlying emotional expression is part of a network involving specific frontal, cingulate, temporal, and parietal areas, as well as the amygdala, the basal ganglia, and thalamus, indicating that this sector of the insula is a site of integration of motor, emotional, sensory and social information. Together with our previous functional studies, this result challenges the classic view of the insula as a multisensory area merely reflecting bodily and internal visceral states. In contrast, it supports an alternative perspective; that the emotional responses classically attributed to the insular cortex are endowed with an enactive component intrinsic to each social and emotional behavior.

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Most of the research on cortical processing of taste has focused on either the primary gustatory cortex (GC) or the orbitofrontal cortex (OFC). However, these are not the only areas involved in taste processing. Gustatory information can also reach another frontal region, the medial prefrontal cortex (mPFC), via direct projections from GC. mPFC has been studied extensively in relation to its role in controlling goal-directed action and reward-guided behaviors, yet very little is known about its involvement in taste coding. The experiments presented here address this important point and test whether neurons in mPFC can significantly process the physiochemical and hedonic dimensions of taste. Spiking responses to intraorally delivered tastants were recorded from rats implanted with bundles of electrodes in mPFC and GC. Analysis of single-neuron and ensemble activity revealed similarities and differences between the two areas. Neurons in mPFC can encode the chemosensory identity of gustatory stimuli. However, responses in mPFC are sparser, more narrowly tuned, and have a later onset than in GC. Although taste quality is more robustly represented in GC, taste palatability is coded equally well in the two areas. Additional analysis of responses in neurons processing the hedonic value of taste revealed differences between the two areas in temporal dynamics and sensitivities to palatability. These results add mPFC to the network of areas involved in processing gustatory stimuli and demonstrate significant differences in taste-coding between GC and mPFC.

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In the last few years, the insula has been the focus of many brain-imaging studies, mostly devoted to clarify its role in emotions and social communication. Physiological data, however, on which one may ground these correlative findings are almost totally lacking. Here, we investigated the functional properties of the insular cortex in behaving monkeys using intracortical microstimulation. Behavioral responses and heart rate changes were recorded. The results showed that the insula is functionally formed by two main subdivisions: (i) a sensorimotor field occupying the caudal-dorsal portion of the insula and appearing as an extension of the parietal lobe; and (ii) a mosaic of orofacial motor programs located in the anterior and centroventral insula sector. These programs show a progressive shift from dorsally located nonemotional motor programs (ingestive activity) to ventral ones laden with emotional and communicative content. The relationship between ingestive and other behaviors is discussed in an evolutionary perspective.

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Evidence from a large number of brain imaging studies has shown that, in humans, the insula, and especially its anterior part, is involved in emotions and emotion recognition. Typically, however, these studies revealed that, besides the insula, a variety of other cortical and subcortical areas are also active. Brain imaging studies are correlative in nature, and, as such, they cannot give indications about the necessary contribution of the different centers involved in emotions. In the present study, we aimed to define more clearly the role of the insula in emotional and social behavior of the monkey by stimulating it electrically. Using this technique, one may determine whether direct activation of the insula can produce specific emotional or social behaviors and exactly which parts of this structure are responsible for these behaviors. The results showed that two emotional behaviors, a basic one (disgust) and a social one (affiliative state), were easily elicited by electrical stimulation of specific parts of the insula. Both behaviors were characterized by specific motor and vegetative responses and by a dramatic change in the monkey's responsiveness to external stimuli.

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Mirror neurons are a distinct class of neurons that discharge both during the execution of a motor act and during observation of the same or similar motor act performed by another individual. However, the extent to which mirror neurons coding a motor act with a specific goal (e.g., grasping) might also respond to the observation of a motor act having the same goal, but achieved with artificial effectors, is not yet established. In the present study, we addressed this issue by recording mirror neurons from the ventral premotor cortex (area F5) of two monkeys trained to grasp objects with pliers. Neuron activity was recorded during the observation and execution of grasping performed with the hand, with pliers and during observation of an experimenter spearing food with a stick. The results showed that virtually all neurons responding to the observation of hand grasping also responded to the observation of grasping with pliers and, many of them to the observation of spearing with a stick. However, the intensity and pattern of the response differed among conditions. Hand grasping observation determined the earliest and the strongest discharge, while pliers grasping and spearing observation triggered weaker responses at longer latencies. We conclude that F5 grasping mirror neurons respond to the observation of a family of stimuli leading to the same goal. However, the response pattern depends upon the similarity between the observed motor act and the one executed by the hand, the natural motor template.

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We recorded motor-evoked potentials (MEPs) to transcranial magnetic stimulation from the right opponens pollicis (OP) muscle while participants observed an experimenter operating two types of pliers: pliers opened by the extension of the fingers and closed by their flexion ("normal pliers") and pliers opened by the flexion of the fingers and closed by their extension ("reverse pliers"). In one experimental condition, the experimenter merely opened and closed the pliers; in the other, he grasped an object with them. In a further condition, the participants imagined themselves operating the normal and reverse pliers. During the observation of actions devoid of a goal, the MEP amplitudes, regardless of pliers used, reflected the muscular pattern involved in the execution of the observed action. In contrast, during the observation of goal-directed actions, the MEPs from OP were modulated by the action goal, increasing during goal achievement despite the opposite hand movements necessary to obtain it. During motor imagery, the MEPs recorded from OP reflected the muscular pattern required to perform the imagined action. We propose that covert activity in the human motor cortex may reflect different aspects of motor behavior. Imagining oneself performing tool actions or observing tool actions devoid of a goal activates the representation of the hand movements that correspond to the observed ones. In contrast, the observation of tool actions with a goal incorporates the distal part of the tool in the observer's body schema, resulting in a higher-order representation of the meaning of the motor act.

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