Lateral habenula neurons signal errors in the prediction of reward information: Humans and animals have the ability to predict future events, which they cultivate by continuously searching their environment for sources of predictive information. However, little is known about the neural systems that motivate this behavior. We hypothesized that information-seeking is assigned value by the same circuits that support reward-seeking, such that neural signals encoding reward prediction errors (RPEs) include analogous information prediction errors (IPEs). To test this, we recorded from neurons in the lateral habenula, a nucleus that encodes RPEs, while monkeys chose between cues that provided different chances to view information about upcoming rewards. We found that a subpopulation of lateral habenula neurons transmitted signals resembling IPEs, responding when reward information was unexpectedly cued, delivered or denied. These signals evaluated information sources reliably, even when the monkey's decisions did not. These neurons could provide a common instructive signal for reward-seeking and information-seeking behavior. Negative reward signals from the lateral habenula to dopamine neurons are mediated by rostromedial tegmental nucleus in primates: Lateral habenula (LHb) neurons signal negative """"""""reward-prediction errors"""""""" and inhibit midbrain dopamine (DA) neurons. Yet LHb neurons are largely glutamatergic, indicating that this inhibition may occur through an intermediate structure. Recent studies in rats have suggested a candidate for this role, the GABAergic rostromedial tegmental nucleus (RMTg), but this neural pathway has not yet been tested directly. We now show using electrophysiology and anatomic tracing that (1) the monkey has an inhibitory structure similar to the rat RMTg;(2) RMTg neurons receive excitatory input from the LHb, exhibit negative reward-prediction errors, and send axonal projections near DA soma;and (3) stimulating this structure inhibits DA neurons. Surprisingly, some RMTg neurons responded to reward cues earlier than the LHb, and carry """"""""state-value"""""""" signals not found in DA neurons. Thus, our data suggest that the RMTg translates LHb reward-prediction errors (negative) into DA reward-prediction errors (positive), while transmitting additional motivational signals to non-DA networks. Regionally distinct processing of rewards and punishments by the primate ventromedial prefrontal cortex: The ventromedial prefrontal cortex (vmPFC) is thought to be related to emotional experience and to the processing of stimulus and action values. However, little is known about how single vmPFC neurons process the prediction and reception of rewards and punishments. We recorded from monkey vmPFC neurons in an experimental situation with alternating blocks, one in which rewards were delivered and one in which punishments were delivered. Many vmPFC neurons changed their activity between blocks. Importantly, neurons in ventral vmPFC were persistently more active in the appetitive """"""""reward"""""""" block, whereas neurons in dorsal vmPFC were persistently more active in the aversive """"""""punishment"""""""" block. Furthermore, within ventral vmPFC, posterior neurons phasically encoded probability of reward, whereas anterior neurons tonically encoded possibility of reward. We found multiple distinct nonlinear valuation mechanisms within the primate prefrontal cortex. Our findings suggest that different subregions of vmPFC contribute differentially to the processing of valence. By conveying such multidimensional and nonlinear signals, the vmPFC may enable flexible control of decisions and emotions to adapt to complex environments. What and where information in the caudate tail guides saccades to visual objects: We understand the world by making saccadic eye movements to various objects. However, it is unclear how a saccade can be aimed at a particular object, because two kinds of visual information, what the object is and where it is, are processed separately in the dorsal and ventral visual cortical pathways. Here, we provide evidence suggesting that a basal ganglia circuit through the tail of the monkey caudate nucleus (CDt) guides such object-directed saccades. First, many CDt neurons responded to visual objects depending on where and what the objects were. Second, electrical stimulation in the CDt induced saccades whose directions matched the preferred directions of neurons at the stimulation site. Third, many CDt neurons increased their activity before saccades directed to the preferred objects and directions of the neurons in a free-viewing condition. Our results suggest that CDt neurons receive both """"""""what"""""""" and """"""""where"""""""" information and guide saccades to visual objects.
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