Lateral habenula neurons signal step-by-step changes of reward prediction

Lee, Hyunchan; Hikosaka, Okihide

doi:10.1016/j.isci.2022.105440

Cited by 6 publications

(4 citation statements)

References 60 publications

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“…Regarding what signals drive this learning, our data is consistent with a model that LHb serves as an aversive teaching signal during CSDS, similar to what has been shown in other settings [33][34][35][36][37][60][61][62] . In particular, we found that: 1) LHb activity was stronger from the first social interactions in the mice that learned more social aversion (i.e.…”

Section: Learning As a Results Of The Csds Paradigmsupporting

confidence: 90%

“…While prior work has uncovered differences between susceptible and resilient mice after CSDS, much less is known about the role of neural teaching signals during stress in driving differences in stress outcomes. Here, we focus on the LHb, which provides a negative teaching signal 32,[56][57][58] and is implicated in aversive learning 33,34 and depression-related behavior 20,34,[37][38][39][59][60][61] , to ask: 1) when and how does activity in the LHb first differ between susceptible and resilient individuals? and 2) do these differences produce behavioral and brainwide correlates of susceptibility?…”

Section: Discussionmentioning

confidence: 99%

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Heightened lateral habenula activity during stress produces brainwide and behavioral substrates of susceptibility

Zhukovskaya,

Christopher,

Willmore

et al. 2023

Preprint

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Some individuals are susceptible to the experience of chronic stress and others are more resilient. While many brain regions implicated in learning are dysregulated after stress, little is known about whether and how neural teaching signals during stress differ between susceptible and resilient individuals. Here, we seek to determine if activity in the lateral habenula (LHb), which encodes a negative teaching signal, differs between stress susceptible and resilient mice during stress to produce different outcomes. After but not before chronic social defeat stress (CSDS), the LHb is active when susceptible mice are in the proximity of the aggressor strain. During stress itself, LHb activity is higher in susceptible mice during aggressor proximity, and stimulation of the LHb during stress biases mice towards susceptibility. This stimulation generates a persistent and widespread increase in the balance of subcortical versus cortical activity that closely mimics the brainwide correlates of susceptibility. Taken together, our results indicate that a stronger aversive teaching signal in the LHb during stress produces brainwide and behavioral substrates of susceptibility.

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Section: Learning As a Results Of The Csds Paradigmsupporting

confidence: 90%

Section: Discussionmentioning

confidence: 99%

Heightened lateral habenula activity during stress produces brainwide and behavioral substrates of susceptibility

Zhukovskaya,

Christopher,

Willmore

et al. 2023

Preprint

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show abstract

“…To address this, we targeted two brain areas that form a junction point between these networks: the lateral habenula (LHb), an ancient epithalamic structure in the RPE network, and the anterior/ventral pallidum (Pal), a basal ganglia output nucleus that projects to the LHb and is part of the information prediction network. The LHb has been heavily implicated in value-related computations due to its strong encoding of RPEs during Pavlovian conditioning and simple decision tasks [27][28][29] , mirroring of and influence over RPE signals in midbrain dopamine neurons 27,30 and causal role in reinforcement learning [31][32][33] . Furthermore, some LHb neurons encode prediction errors for both juice reward and information (for example, excited by 'less juice than predicted' and also 'less information than predicted'), suggesting that they could integrate multiple forms of reward into a common currency of value 26 .…”

Section: Conserved Information Value In Humans Monkeys Pal and Lhbmentioning

confidence: 99%

A neural mechanism for conserved value computations integrating information and rewards

Bromberg-Martin,

Feng,

Ogasawara

et al. 2024

Nat Neurosci

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Behavioral and economic theory dictate that we decide between options based on their values. However, humans and animals eagerly seek information about uncertain future rewards, even when this does not provide any objective value. This implies that decisions are made by endowing information with subjective value and integrating it with the value of extrinsic rewards, but the mechanism is unknown. Here, we show that human and monkey value judgements obey strikingly conserved computational principles during multi-attribute decisions trading off information and extrinsic reward. We then identify a neural substrate in a highly conserved ancient structure, the lateral habenula (LHb). LHb neurons signal subjective value, integrating information’s value with extrinsic rewards, and the LHb predicts and causally influences ongoing decisions. Neurons in key input areas to the LHb largely signal components of these computations, not integrated value signals. Thus, our data uncover neural mechanisms of conserved computations underlying decisions to seek information about the future.

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“…The reward prediction error can be positive or negative, depending on whether the actual reward is bigger than prediction. The positive and negative reward prediction error signals can be widely found in lateral habenula neurons, or the specific neurons in striatum, globus pallidus, amygdala, anterior cingulate cortex and supplementary eye field (Bermudez and Schultz, 2010;So and Stuphorn, 2012;Schroll et al, 2015;Schultz, 2017;Alexander and Brown, 2019;Lee and Hikosaka, 2022;Basanisi et al, 2023). Dopaminergic neurons in VTA can induce conditioned place preference (Tsai et al, 2009), which indicates better context associations based on reward (McKendrick and Graziane, 2020).…”

Section: Dopaminergic Neurons Encode Reward Prediction Error Signalmentioning

confidence: 99%

Reward prediction error in learning-related behaviors

Deng,

Song,

et al. 2023

Front. Neurosci.

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Learning is a complex process, during which our opinions and decisions are easily changed due to unexpected information. But the neural mechanism underlying revision and correction during the learning process remains unclear. For decades, prediction error has been regarded as the core of changes to perception in learning, even driving the learning progress. In this article, we reviewed the concept of reward prediction error, and the encoding mechanism of dopaminergic neurons and the related neural circuities. We also discussed the relationship between reward prediction error and learning-related behaviors, including reversal learning. We then demonstrated the evidence of reward prediction error signals in several neurological diseases, including Parkinson’s disease and addiction. These observations may help to better understand the regulatory mechanism of reward prediction error in learning-related behaviors.

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Lateral habenula neurons signal step-by-step changes of reward prediction

Cited by 6 publications

References 60 publications

Heightened lateral habenula activity during stress produces brainwide and behavioral substrates of susceptibility

Heightened lateral habenula activity during stress produces brainwide and behavioral substrates of susceptibility

A neural mechanism for conserved value computations integrating information and rewards

Reward prediction error in learning-related behaviors

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