The Globus Pallidus Sends Reward-Related Signals to the Lateral Habenula

Hong, Simon; Hikosaka, Okihide

doi:10.1016/j.neuron.2008.09.035

Cited by 287 publications

(322 citation statements)

References 39 publications

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“…4I). The striosomes may, therefore, be the source of reward-related information that inhibits the habenula-projecting pallidal neurons in response to reward or reward prediction (5,14).…”

Section: Gph and Gpi/gpe Neurons Differ In Their Electrophysiologicalmentioning

confidence: 99%

mentioning

confidence: 99%

“…Recent in vivo recordings in primates have shown that the activity of these habenula-projecting pallidal neurons is modulated by the cues that predict the availability of reward (13,14) and not by aspects of movements. The majority of these pallidal neurons, as with lateral habenula neurons, are excited in response to errors in reward prediction or in expectation of an adverse outcome (14,15). In addition, selective activation of this pallido-habenula projection in rodents can induce aversive conditioning (16) and activation of the lateral habenula can devalue a rewarding stimulus (17).…”

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confidence: 99%

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Independent circuits in the basal ganglia for the evaluation and selection of actions

Stephenson-Jones

Kardamakis

Robertson

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

116

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The basal ganglia are critical for selecting actions and evaluating their outcome. Although the circuitry for selection is well understood, how these nuclei evaluate the outcome of actions is unknown. Here, we show in lamprey that a separate evaluation circuit, which regulates the habenula-projecting globus pallidus (GPh) neurons, exists within the basal ganglia. The GPh neurons are glutamatergic and can drive the activity of the lateral habenula, which, in turn, provides an indirect inhibitory influence on midbrain dopamine neurons. We show that GPh neurons receive inhibitory input from the striosomal compartment of the striatum. The striosomal input can reduce the excitatory drive to the lateral habenula and, consequently, decrease the inhibition onto the dopaminergic system. Dopaminergic neurons, in turn, provide feedback that inhibits the GPh. In addition, GPh neurons receive direct projections from the pallium (cortex in mammals), which can increase the GPh activity to drive the lateral habenula to increase the inhibition of the neuromodulatory systems. This circuitry, thus, differs markedly from the "direct" and "indirect" pathways that regulate the pallidal (e.g., globus pallidus) output nuclei involved in the control of motion. Our results show that a distinct reward-evaluation circuit exists within the basal ganglia, in parallel to the direct and indirect pathways, which select actions. Our results suggest that these circuits are part of the fundamental blueprint that all vertebrates use to select actions and evaluate their outcome.striosomes | reward/aversion | pallium/cortex | evolution T o achieve a goal, animals need to select actions and evaluate their outcome to determine whether their goal was achieved. In mammals, the basal ganglia play a key role in the selection of actions (1-3) and have more recently been suggested to additionally contribute to predicting and evaluating the outcome of the selected actions (4-8).The so-called "direct" and "indirect" pathways through the basal ganglia are present in all vertebrates and act together to select actions by decreasing tonic inhibition of the basal ganglia output nuclei [globus pallidus interna (GPi) and substantia nigra pars reticulata (SNr)] on a selected motor program and increasing the inhibition onto other competing actions. The output of these selection circuits target brainstem and thalamic motor areas, and neurons within this circuit are modulated by various aspect of movement kinetics related to the initiation and modulation of ongoing actions.In addition to the output neurons that project to motor areas, a separate subpopulation of pallidal neurons projects to the lateral habenula (9-12), a structure involved in evaluating and predicting the motivational value of actions. Recent in vivo recordings in primates have shown that the activity of these habenula-projecting pallidal neurons is modulated by the cues that predict the availability of reward (13,14) and not by aspects of movements. The majority of these pallidal neurons, as with latera...

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“…4I). The striosomes may, therefore, be the source of reward-related information that inhibits the habenula-projecting pallidal neurons in response to reward or reward prediction (5,14).…”

Section: Gph and Gpi/gpe Neurons Differ In Their Electrophysiologicalmentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

See 1 more Smart Citation

Independent circuits in the basal ganglia for the evaluation and selection of actions

Stephenson-Jones

Kardamakis

Robertson

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

116

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“…With these designs, we identified activations in posterior striatal regions, extending into the globus pallidus. The globus pallidus codes reward, receives inputs primarily from the ventral striatum, and sends rewardrelated information to the lateral habenula, which in turn innervates dopamine neurons (48,49). Critically, the distinction between striatal and lateral prefrontal responses suggests that not all expected value-sensitive regions integrate risk.…”

Section: Individual Differences In Risk Processingmentioning

confidence: 99%

Risk-dependent reward value signal in human prefrontal cortex

Tobler

Christopoulos

O’Doherty

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

163

141

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When making choices under uncertainty, people usually consider both the expected value and risk of each option, and choose the one with the higher utility. Expected value increases the expected utility of an option for all individuals. Risk increases the utility of an option for risk-seeking individuals, but decreases it for risk averse individuals. In 2 separate experiments, one involving imperative (no-choice), the other choice situations, we investigated how predicted risk and expected value aggregate into a common reward signal in the human brain. Blood oxygen level dependent responses in lateral regions of the prefrontal cortex increased monotonically with increasing reward value in the absence of risk in both experiments. Risk enhanced these responses in risk-seeking participants, but reduced them in risk-averse participants. The aggregate value and risk responses in lateral prefrontal cortex contrasted with pure value signals independent of risk in the striatum. These results demonstrate an aggregate risk and value signal in the prefrontal cortex that would be compatible with basic assumptions underlying the mean-variance approach to utility. decision making ͉ fMRI ͉ utility ͉ mean-variance approach ͉ neuroeconomics

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“…Indeed, GAD67 is expressed in all subpallial regions in zebrafish (figure 1b) [5]. In particular, the entopeduncular nucleus (EN) has been identified as equivalent to the mammalian globus pallidus internal segment (GPi), which gives rise to the BG output to the thalamus and habenula [4,11]. In rodents, primates and humans, the dorsal striatum is essential for time keeping [12][13][14].…”

Section: Introductionmentioning

confidence: 99%

Zebrafish forebrain and temporal conditioning

Cheng

Jesuthasan

Penney

2014

Phil. Trans. R. Soc. B

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The rise of zebrafish as a neuroscience research model organism, in conjunction with recent progress in single-cell resolution whole-brain imaging of larval zebrafish, opens a new window of opportunity for research on interval timing. In this article, we review zebrafish neuroanatomy and neuromodulatory systems, with particular focus on identifying homologies between the zebrafish forebrain and the mammalian forebrain. The neuroanatomical and neurochemical basis of interval timing is summarized with emphasis on the potential of using zebrafish to reveal the neural circuits for interval timing. The behavioural repertoire of larval zebrafish is reviewed and we demonstrate that larval zebrafish are capable of expecting a stimulus at a precise time point with minimal training. In conclusion, we propose that interval timing research using zebrafish and whole-brain calcium imaging at single-cell resolution will contribute to our understanding of how timing and time perception originate in the vertebrate brain from the level of single cells to circuits.

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The Globus Pallidus Sends Reward-Related Signals to the Lateral Habenula

Cited by 287 publications

References 39 publications

Independent circuits in the basal ganglia for the evaluation and selection of actions

Independent circuits in the basal ganglia for the evaluation and selection of actions

Risk-dependent reward value signal in human prefrontal cortex

Zebrafish forebrain and temporal conditioning

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