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The habenula is present in vertebrate brains but its function has remained obscure. Okihide Hikosaka reviews data from animal and human studies that indicate that the habenula, through its effects on dopamine and serotonin systems, regulates motor suppression in various contexts.

Neurons in the primate lateral habenula are shown to have reward-related activity that apparently signals the inverse to the dopamine response. Stimulation of lateral habenula suppresses dopamine neurons, suggesting that this area plays a role in shaping reward signals.

The observation that midbrain dopamine neurons are activated by reward, or sensory stimuli predicting reward, has led to the hypothesis that they encode value-related signals and are inhibited by aversive events. This is now shown to be true for only a subset of dopamine neurons; by recording neuronal activity in monkeys, dopamine neurons are found to be more heterogeneous than this model would suggest.

How the primate dopamine system retains information on higher-order factors such as environmental context remains elusive. Here, the authors show tonic activity changes of dopamine neurons in different environments and the involvement of a putative amygdala-nigra pathway in such neural modulation.

How object salience is encoded in the cortex and basal ganglia remains incompletely understood. Here, the authors show that individual prefrontal cortex neurons are jointly sensitive to the memory of value, aversiveness, novelty, and recency of objects, while the substantia nigra reticulata filters out novelty and recency signals but amplifies value and aversive memories.

In this review, the authors discuss the role of the lateral habenula in processing reward, both in the healthy brain and in models of depression, drawing on work in non-human primates and rodents.

The caudate tail encodes the stable value associated with visual objects and modulates gaze accordingly. Here, the authors use pathway-specific optogenetic manipulation of the caudate terminals in the substantia nigra pars reticulata on oculomotor behaviour.

Making informed decisions requires taking into account how reliably choices produce expected outcomes. This study shows that primate anterodorsal septal neurons encode an uncertainty signal sensitive to reward size but do not carry information about the uncertainty of punishments.

The authors report that the population of lateral habenula neurons responds most strongly for the most unpleasant outcome in a particular context: either the absence of reward when rewards are available or the presence of punishment when punishments are feared.

Humans and animals value information that can help them predict future events. Here, the authors test whether the value of information is encoded in the same way as the value of rewards. They find signals in the lateral habenula that could provide a common instructive signal for reward-seeking and information-seeking behavior.