Diverse sources of reward value signals in the basal ganglia nuclei transmitted to the lateral habenula in the monkey

AbstractActivation of the subthalamic nucleus (STN) is associated with the stopping of ongoing behavior via the basal ganglia. However, we recently observed that optogenetic STN excitation induced a strong jumping/escaping behavior. We hypothesized that STN activation is aversive. To test this, place preference was assessed. Optogenetic excitation of the STN caused potent place aversion. Causality between STN activation and aversion has not been demonstrated previously. The lateral habenula (LHb) is a critical hub for aversion. Optogenetic stimulation of the STN indeed caused firing of LHb neurons, but with delay, suggesting the involvement of a polysynaptic circuit. To unravel a putative pathway, the ventral pallidum (VP) was investigated. VP receives projections from the STN and in turn projects to the LHb. Optogenetic excitation of STN-VP terminals caused firing of VP neurons and induced aversive behavior. This study identifies the STN as critical hub for aversion, potentially mediated via an STN-VP-LHb pathway.

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The orbitofrontal cortex, amygdala, reward value, and emotion

Brain Computations ◽

10.1093/oso/9780198871101.003.0011 ◽

2020 ◽

pp. 379-446

Author(s):

Edmund T. Rolls

Keyword(s):

Neural Networks ◽

Decision Making ◽

Basal Ganglia ◽

Anterior Cingulate Cortex ◽

Orbitofrontal Cortex ◽

Brain Region ◽

Anterior Cingulate ◽

Rule Based ◽

Reward Value ◽

Trial Object

The orbitofrontal cortex receives from the ends of all sensory processing systems, and converts these representations of what the stimulus is into representations of their reward value. The orbitofrontal cortex is therefore a key brain region in emotions, which can be defined as states elicited by rewards and punishers. Indeed, orbitofrontal cortex activations are linearly related to the subjectively reported pleasantness of stimuli. The orbitofrontal cortex then projects this reward value information to other structures, which implement behavioural output, such as the anterior cingulate cortex, and the basal ganglia. A key computational capacity of the orbitofrontal cortex is one-trial object-reward associations, which are rule-based, and enable primates including humans to change their rewarded behaviour very rapidly. Decision-making using attractor neural networks is described.

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A Pallidus-Habenula-Dopamine Pathway Signals Inferred Stimulus Values

Journal of Neurophysiology ◽

10.1152/jn.00158.2010 ◽

2010 ◽

Vol 104 (2) ◽

pp. 1068-1076 ◽

Cited By ~ 100

Author(s):

Ethan S. Bromberg-Martin ◽

Masayuki Matsumoto ◽

Simon Hong ◽

Okihide Hikosaka

Keyword(s):

Reinforcement Learning ◽

Dopamine Neurons ◽

Neural Pathway ◽

Dopamine System ◽

Lateral Habenula ◽

Reward Value ◽

Saccade Task ◽

Midbrain Dopamine ◽

Behavioral Evidence ◽

Midbrain Dopamine Neurons

The reward value of a stimulus can be learned through two distinct mechanisms: reinforcement learning through repeated stimulus-reward pairings and abstract inference based on knowledge of the task at hand. The reinforcement mechanism is often identified with midbrain dopamine neurons. Here we show that a neural pathway controlling the dopamine system does not rely exclusively on either stimulus-reward pairings or abstract inference but instead uses a combination of the two. We trained monkeys to perform a reward-biased saccade task in which the reward values of two saccade targets were related in a systematic manner. Animals used each trial's reward outcome to learn the values of both targets: the target that had been presented and whose reward outcome had been experienced (experienced value) and the target that had not been presented but whose value could be inferred from the reward statistics of the task (inferred value). We then recorded from three populations of reward-coding neurons: substantia nigra dopamine neurons; a major input to dopamine neurons, the lateral habenula; and neurons that project to the lateral habenula, located in the globus pallidus. All three populations encoded both experienced values and inferred values. In some animals, neurons encoded experienced values more strongly than inferred values, and the animals showed behavioral evidence of learning faster from experience than from inference. Our data indicate that the pallidus-habenula-dopamine pathway signals reward values estimated through both experience and inference.

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Evidence for a dopaminergic innervation of the cat lateral habenula: its role in controlling serotonin transmission in the Basal ganglia

Brain Research ◽

10.1016/0006-8993(84)91067-9 ◽

1984 ◽

Vol 308 (2) ◽

pp. 281-288 ◽

Cited By ~ 12

Author(s):

T.D. Reisine ◽

P. Soubrié ◽

A. Ferron ◽

C. Blas ◽

R. Romo ◽

...

Keyword(s):

Basal Ganglia ◽

Lateral Habenula

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Neuronal Encoding of Reward Value and Direction of Actions in the Primate Putamen

Journal of Neurophysiology ◽

10.1152/jn.00104.2009 ◽

2009 ◽

Vol 102 (6) ◽

pp. 3530-3543 ◽

Cited By ~ 29

Author(s):

Yukiko Hori ◽

Takafumi Minamimoto ◽

Minoru Kimura

Keyword(s):

Basal Ganglia ◽

Large Reward ◽

Small Reward ◽

Button Press ◽

Projection Neurons ◽

Discharge Rates ◽

Reward Value ◽

External Events ◽

Neuronal Encoding ◽

Response Direction

Decision making and action selection are influenced by the values of benefit, reward, cost, and punishment. Mapping of the positive and negative values of external events and actions occurs mainly via the discharge rates of neurons in the cerebral cortex, the amygdala, and the basal ganglia. However, it remains unclear how the reward values of external events and actions encoded in the basal ganglia are integrated into reward value-based control of limb-movement actions through the corticobasal ganglia loops. To address this issue, we investigated the activities of presumed projection neurons in the putamen of macaque monkeys performing a visually instructed GO–NOGO button-press task for large and small rewards. Regression analyses of neuronal discharge rates, actions, and reward values revealed three major categories of neurons. First, neurons activated during the preinstruction delay period were selective to either the GO(large reward)–NOGO(small reward) or NOGO(large reward)–GO(small reward) combinations, although the actions to be instructed were not predictable. Second, during the postinstruction epoch, GO and NOGO action-related activities were highly selective to reward size. The pre- and postinstruction activities of a large subset of neurons were also selective to cue position or GO-response direction. Third, neurons activated during both the pre- and postinstruction epochs were selective to both action and reward size. The results support the view that putamen neurons encode reward value and direction of actions, which may be a basis for mediating the processes leading from reward-value mapping to guiding ongoing actions toward their expected outcomes and directions.

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The habenula-targeting neurons in the mouse entopeduncular nucleus contain not only somatostatin-positive neurons but also nitric oxide synthase-positive neurons

Brain Structure and Function ◽

10.1007/s00429-021-02264-1 ◽

2021 ◽

Author(s):

Yuta Miyamoto ◽

Takaichi Fukuda

Keyword(s):

Nitric Oxide ◽

Basal Ganglia ◽

Nitric Oxide Synthase ◽

Core Region ◽

Entopeduncular Nucleus ◽

Double Positive ◽

Lateral Habenula ◽

Aversive Stimuli ◽

Oxide Synthase ◽

Shell Region

AbstractThe entopeduncular nucleus (EPN) in rodents is one of the two major output nuclei of the basal ganglia and corresponds to the internal segment of the globus pallidus in primates. Previous studies have shown that the EPN contains three types of neurons that project to different targets, namely, parvalbumin (PV)-, somatostatin (SOM)-, and choline acetyltransferase-positive neurons. However, we have recently reported that neurons lacking immunoreactivities for these substances are present in the EPN. Here, we demonstrate that 27.7% of all EPN neurons showed immunoreactivity for nitric oxide synthase (NOS). Among them, NOS-only positive and NOS/SOM double-positive neurons accounted for 20.1% and 6.8%, respectively, whereas NOS/PV double-positive neurons were rarely observed. NOS-containing neurons were distributed in a shell region surrounding the thalamus-targeting, PV-rich core region of the EPN, especially in the ventromedial part of the shell. The retrograde tracer fluoro-gold (FG) was injected into several target regions of EPN neurons. Among FG-labeled EPN neurons after injection into the lateral habenula (LHb), NOS-only positive, NOS/SOM double-positive, and SOM-only positive neurons accounted for 25.7%, 15.2%, and 59.1%, respectively. We conclude that NOS-positive neurons are the second major population of LHb-targeting EPN neurons, suggesting their possible involvement in behaviors in response to aversive stimuli.

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