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| Open AccessChronic nicotine increases midbrain dopamine neuron activity and biases individual strategies towards reduced exploration in mice
Chronic nicotine exposure impacts various components of decision-making processes, such as exploratory behaviors. Here, the authors identify the cellular mechanism and show that chronic nicotine exposure increases the tonic activity of VTA dopaminergic neurons and reduces exploration in mice.
- Malou Dongelmans
- , Romain Durand-de Cuttoli
- & Philippe Faure
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Article
| Open AccessEntropy-based metrics for predicting choice behavior based on local response to reward
Animals distribute their choices between alternative options according to relative reinforcement they receive from those options (matching law). Here, the authors propose metrics based on information theory that can predict this global behavioral rule based on local response to reward feedback.
- Ethan Trepka
- , Mehran Spitmaan
- & Alireza Soltani
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| Open AccessMid-lateral cerebellar complex spikes encode multiple independent reward-related signals during reinforcement learning
The role of complex spikes in reinforcement learning is still unclear. Here, the authors show that complex spikes carry multiple context based, cell type specific and learning dependent signals that are independent of changes in any motor kinematics and unlikely to instruct the concurrent simple spike activity during reinforcement learning.
- Naveen Sendhilnathan
- , Anna Ipata
- & Michael E. Goldberg
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| Open AccessZebrafish capable of generating future state prediction error show improved active avoidance behavior in virtual reality
Using a closed-loop virtual reality system for fish, the authors show that zebrafish are capable of assigning rules to the scenery they see, and of generating a state prediction error by comparing reality with a prediction derived from an internal model.
- Makio Torigoe
- , Tanvir Islam
- & Hitoshi Okamoto
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| Open AccessChoice-relevant information transformation along a ventrodorsal axis in the medial prefrontal cortex
Choice-relevant computations across the medial prefrontal cortex differ only quantitatively between areas. Here the authors suggest these computations may be organized along a functional gradient.
- David J.-N. Maisson
- , Tyler V. Cash-Padgett
- & Jan Zimmermann
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| Open AccessNeural and computational mechanisms of momentary fatigue and persistence in effort-based choice
The willingness to exert effort into demanding tasks often declines over time through fatigue. Here the authors provide a computational account of the moment-to-moment dynamics of fatigue and its impact on effort-based choices, and reveal the neural mechanisms that underlie such computations.
- Tanja Müller
- , Miriam C. Klein-Flügge
- & Matthew A. J. Apps
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Article
| Open AccessThe tectonigral pathway regulates appetitive locomotion in predatory hunting in mice
Goal-oriented movement is a fundamental animal behaviour. Here, the authors show that neurons in the superior colliculus project to the substantia nigra pars compacta, regulating dopaminergic signaling and specifically appetitive locomotion in mice.
- Meizhu Huang
- , Dapeng Li
- & Peng Cao
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Article
| Open AccessReward biases spontaneous neural reactivation during sleep
Sleep is known to promote memory consolidation, but the extent to which this is dependent on the memory’s relevance remains unclear. Here, the authors use a brain decoding approach to show that neural representations of rewarded experiences undergo a privileged reactivation during sleep, favouring their consolidation.
- Virginie Sterpenich
- , Mojca K. M. van Schie
- & Sophie Schwartz
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| Open AccessVentral tegmental area GABA neurons mediate stress-induced blunted reward-seeking in mice
Acute stress transiently disrupts reward-seeking behaviour and repeated stress exposure produces lasting anhedonia-like behaviour in rodents. Here, the authors show that stress triggers GABAergic activity in the ventral tegmental area which blunts reward-seeking behaviour in mice.
- Daniel C. Lowes
- , Linda A. Chamberlin
- & Alexander Z. Harris
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Article
| Open AccessAnatomical dissociation of intracerebral signals for reward and punishment prediction errors in humans
Whether maximizing rewards and minimizing punishments rely on distinct brain learning systems remains debated. Here, using intracerebral recordings in humans, the authors provide evidence for brain regions differentially engaged in signaling reward and punishment prediction errors that prescribe repetition versus avoidance of past choices.
- Maëlle C. M. Gueguen
- , Alizée Lopez-Persem
- & Julien Bastin
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| Open AccessTransforming absolute value to categorical choice in primate superior colliculus during value-based decision making
Value-based decision making involves choosing from multiple options with different values. The authors identify a neural mechanism that directly transforms absolute values to categorical choices within the superior colliculus and which supports value-based decision making critical for real-world economic behaviours.
- Beizhen Zhang
- , Janis Ying Ying Kan
- & Michael Christopher Dorris
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Article
| Open AccessSupramammillary neurons projecting to the septum regulate dopamine and motivation for environmental interaction in mice
The supramammillary region (SuM) regulates arousal that reinforces and energizes behavioral interaction with the environment. Here the authors investigate how SuM neurons interact with medial septal neurons and ventral tegmental dopamine neurons to regulate motivation for environmental interaction.
- Andrew J. Kesner
- , Rick Shin
- & Satoshi Ikemoto
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Article
| Open AccessLearning with reinforcement prediction errors in a model of the Drosophila mushroom body
Dopamine neurons in the mushroom body help Drosophila learn to approach rewards and avoid punishments. Here, the authors propose a model in which dopaminergic learning signals encode reinforcement prediction errors by utilising feedback reinforcement predictions from mushroom body output neurons.
- James E. M. Bennett
- , Andrew Philippides
- & Thomas Nowotny
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Article
| Open AccessInput-specific modulation of murine nucleus accumbens differentially regulates hedonic feeding
Hedonic feeding occurs in the absence of metabolic need and plays a critical role in the excessive feeding that underlies obesity. The authors show that optogenetic manipulation of NAc inputs from the prefrontal cortex versus inputs from the anterior paraventricular nucleus of the thalamus has opposite effects on high fat intake.
- Daniel J. Christoffel
- , Jessica J. Walsh
- & Robert C. Malenka
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Article
| Open AccessMulticentric tracking of multiple agents by anterior cingulate cortex during pursuit and evasion
Pursuit or evasion requires world-centric and agent-centric representation to coordinate navigation and motor control. The dorsal anterior cingulate cortex, which communicates bi-directionally with both the hippocampal complex and premotor areas serve a mapping role in this process.
- Seng Bum Michael Yoo
- , Jiaxin Cindy Tu
- & Benjamin Yost Hayden
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| Open AccessDissociable roles of cortical excitation-inhibition balance during patch-leaving versus value-guided decisions
Here, the authors show that the balance between excitation and inhibition in two cortical areas is differentially related to maximizing immediate rewards, and to weighting the cost against long-term gains of moving to a new environment.
- Luca F. Kaiser
- , Theo O. J. Gruendler
- & Gerhard Jocham
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Article
| Open AccessDistinct populations of cortical pyramidal neurons mediate drug reward and aversion
The anterior cingulate plays a role in addiction, but studies have not examined the role of its two types of glutamatergic projection neurons, pyramidal tract (PT) and intratelencephalic (IT). Here we demonstrate that these two populations regulate distinct features of a drug experience, its positive and negative aspects, respectively.
- A. F. Garcia
- , E. A. Crummy
- & S. M. Ferguson
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Article
| Open AccessEndocannabinoid signaling regulates the reinforcing and psychostimulant effects of ketamine in mice
Ketamine is used for sedation and treatment of depression, but is also a drug of abuse. Here the authors show that ketamine modulates the endocannabinoid system in mice, and that this may contribute to its psychoactive effects.
- Wei Xu
- , Hongchun Li
- & Xiaobo Cen
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Article
| Open AccessSensory substitution reveals a manipulation bias
The challenge of sensory substitution as a therapeutic approach is to design systems that are well accepted by subjects. Here, in deaf songbirds, the authors substitute hearing with vision, suggesting substitution devices could provide sensory feedback for the key actions that are deprived.
- Anja T. Zai
- , Sophie Cavé-Lopez
- & Richard H. R. Hahnloser
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| Open AccessDistinct dynamics of social motivation drive differential social behavior in laboratory rat and mouse strains
Laboratory rat and mouse strains serve as animal models to explore brain mechanisms underlying social behavior. Here, the authors describe differences in social behavior between commonly used rat and mouse strains, which may reflect distinct dynamics of social motivation.
- Shai Netser
- , Ana Meyer
- & Shlomo Wagner
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| Open AccessDifferential reinforcement encoding along the hippocampal long axis helps resolve the explore–exploit dilemma
Decisions under uncertainty involve a balance between exploiting familiar valuable options and exploring unfamiliar ones. Here, the authors study hippocampal responses using fMRI during a reinforcement learning task, and show the differential involvement of the anterior-posterior regions in the explore-exploit aspects of the task.
- Alexandre Y. Dombrovski
- , Beatriz Luna
- & Michael N. Hallquist
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Article
| Open AccessAutomated markerless pose estimation in freely moving macaques with OpenMonkeyStudio
The rhesus macaque is an important model species in several branches of science, but the utility of this model would be enhanced by the ability to measure behaviour throughout pose. Here, the authors describe a deep learning-based markerless motion capture system for estimating 3D pose in freely moving macaques.
- Praneet C. Bala
- , Benjamin R. Eisenreich
- & Jan Zimmermann
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Article
| Open AccessCocaine-mediated circadian reprogramming in the striatum through dopamine D2R and PPARγ activation
Drugs of abuse have been shown to perturb circadian rhythms. Here, the authors show in mice that cocaine exposure modulates circadian gene expression in the striatum through a previously unappreciated pathway that involves dopamine D2 receptors and the nuclear receptor PPARγ.
- Karen Brami-Cherrier
- , Robert G. Lewis
- & Emiliana Borrelli
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Article
| Open AccessMolecular layer interneurons in the cerebellum encode for valence in associative learning
This study shows that cerebellar molecular layer interneurons (MLIs) develop responses encoding for identity of the stimulus in an associative learning task. Chemogenetic inhibition of MLIs decreased the ability of mice to discriminate stimuli suggesting that MLIs encode for stimulus valence.
- Ming Ma
- , Gregory L. Futia
- & Diego Restrepo
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| Open AccessDissociable mesolimbic dopamine circuits control responding triggered by alcohol-predictive discrete cues and contexts
Alcohol craving can be enhanced by alcohol-associated cues and by alcohol-associated contexts. Here the authors investigate the role of the ventral tegmental area (VTA)-to-nucleus accumbens (NAc) core and VTA-to-NAc shell circuits in mediating these distinct aspects of alcohol seeking behaviour in rats.
- Milan D. Valyear
- , Iulia Glovaci
- & Nadia Chaudhri
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| Open AccessVagus nerve stimulation boosts the drive to work for rewards
The vagus nerve transmits signals between the gut and the brain thereby tuning motivated behavior to physiological needs. Here, the authors show that acute non-invasive stimulation of the vagus nerve via the ear enhances the invigoration of effort for rewards.
- Monja P. Neuser
- , Vanessa Teckentrup
- & Nils B. Kroemer
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Article
| Open AccessValue and choice as separable and stable representations in orbitofrontal cortex
In value-based decision-making, single prefrontal neurons represent multiple variables at different times in the decision process. Here, the authors show these representations to be separable and stable at the population level, allowing read out of specific variables at behaviorally relevant times.
- Daniel L. Kimmel
- , Gamaleldin F. Elsayed
- & William T. Newsome
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Article
| Open AccessPhasic dopamine reinforces distinct striatal stimulus encoding in the olfactory tubercle driving dopaminergic reward prediction
It is not entirely understood how network plasticity produces the coding of predicted value during stimulus-outcome learning. Here, the authors reveal a reinforcing loop in distributed limbic circuits, transforming sensory stimuli into reward prediction coding broadcasted by dopamine neurons to the brain.
- Lars-Lennart Oettl
- , Max Scheller
- & Wolfgang Kelsch
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Article
| Open AccessBiased belief updating and suboptimal choice in foraging decisions
In some types of decision-making, people must accept or forego an option without knowing what prospects might later be available. Here, the authors reveal how a key bias– asymmetric learning from negative versus positive outcomes – emerges in this type of decision.
- Neil Garrett
- & Nathaniel D. Daw
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| Open AccessThe role of mPFC and MTL neurons in human choice under goal-conflict
Optimizing approach-avoidance behavior calls for neural encoding of related motivation outcomes. Here, the authors show that behavioral choice under conflict relies on differential neuronal firing patterns after punishment, in which mPFC neurons decode the outcome’s value and MTL neurons follow by reducing subsequent approach.
- Tomer Gazit
- , Tal Gonen
- & Itzhak Fried
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| Open AccessThe central amygdala recruits mesocorticolimbic circuitry for pursuit of reward or pain
Brain disorders can create maladaptive attractions, such as in addiction or self-harming. Here the authors use multiple valence modes of the central amygdala to create such attractions, arbitrarily making rats into ‘sucrose addicts' or ‘cocaine addicts', or causing maladaptive attraction to shocks.
- Shelley M. Warlow
- , Erin E. Naffziger
- & Kent C. Berridge
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| Open AccessRepresentation of probabilistic outcomes during risky decision-making
Goal directed behavior requires the sequential retrieval and evaluation of the multiple choices for action and their deterministic outcomes. Here, the authors report sequential, decodable probabilistic outcome representations in magnetoencephalography (MEG) signals during a risky foraging task.
- Giuseppe Castegnetti
- , Athina Tzovara
- & Dominik R. Bach
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| Open AccessMouse tracking reveals structure knowledge in the absence of model-based choice
Mouse tracking can reveal people’s subjective beliefs and whether they understand the structure of a task. These data demonstrate that people often do not use this information to make good choices.
- Arkady Konovalov
- & Ian Krajbich
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Article
| Open AccessMicroglial activation increases cocaine self-administration following adolescent nicotine exposure
Adolescents are particularly sensitive to nicotine. Here the authors show that in mice, microglial activation contributes to the enhanced sensitivity to cocaine caused by nicotine exposure in young mice.
- K. E. Linker
- , M. Gad
- & F. M. Leslie
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Article
| Open AccessDopamine transients do not act as model-free prediction errors during associative learning
Dopamine neurons are proposed to signal the reward prediction error in model-free reinforcement learning algorithms. Here, the authors show that when given during an associative learning task, optogenetic activation of dopamine neurons causes associative, rather than value, learning.
- Melissa J. Sharpe
- , Hannah M. Batchelor
- & Geoffrey Schoenbaum
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Article
| Open AccessControllability governs the balance between Pavlovian and instrumental action selection
Pavlovian and instrumentally driven actions often conflict when determining the best outcome. Here, the authors present an arbitration theory supported by human behavioral data where Pavlovian predictors drive action selection in an uncontrollable environment, while more flexible instrumental prediction dominates under conditions of high controllability.
- Hayley M. Dorfman
- & Samuel J. Gershman
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| Open AccessKetamine can reduce harmful drinking by pharmacologically rewriting drinking memories
Memories linking environmental cues to alcohol reward are involved in the development and maintenance of heavy drinking. Here, the authors show that a single dose of ketamine, given after retrieval of alcohol-reward memories, disrupts the reconsolidation of these memories and reduces drinking in humans.
- Ravi K. Das
- , Grace Gale
- & Sunjeev K. Kamboj
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| Open AccessGoal congruency dominates reward value in accounting for behavioral and neural correlates of value-based decision-making
Decision-making research has confounded the reward value of options with their goal-congruency, as the task goal was always to pick the most rewarding option. Here, authors separately asked participants to select the least rewarding of a set of options, revealing a dominant role for goal congruency.
- Romy Frömer
- , Carolyn K. Dean Wolf
- & Amitai Shenhav
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| Open AccessOrbitofrontal signals for two-component choice options comply with indifference curves of Revealed Preference Theory
Recording from monkey orbitofrontal cortex, the authors used composite reward bundles and found individual neuron and population responses that were suitable for economic choice. The responses followed behavioral indifference curves and predicted behavioral choices consistent with formalisms of Revealed Preference Theory.
- Alexandre Pastor-Bernier
- , Arkadiusz Stasiak
- & Wolfram Schultz
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| Open AccessMultiple associative structures created by reinforcement and incidental statistical learning mechanisms
Associative learning occurs through reinforcement mechanisms as well as incidentally through experience of statistical relationships. Here, the authors report that these two learning processes are associated with specialized anatomical regions that operate at different time scales.
- Miriam C. Klein-Flügge
- , Marco K. Wittmann
- & Matthew F. S. Rushworth
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Article
| Open AccessNMDA receptor-dependent plasticity in the nucleus accumbens connects reward-predictive cues to approach responses
Conditioned stimuli elicit phasic changes in nucleus accumbens (NAc) firing that invigorate approach responses to predicted rewards. Here the authors show that NAc neurons acquire cue-evoked responses during learning as a result of excitatory plasticity within the NAc.
- Mercedes Vega-Villar
- , Jon C. Horvitz
- & Saleem M. Nicola
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Article
| Open AccessPlasticity in striatal dopamine release is governed by release-independent depression and the dopamine transporter
Dopamine release in the striatum has important roles in action selection and in disorders such as Parkinson’s disease. The authors here show that short-term plasticity of dopamine release is strongly determined by axonal activation and dopamine transporters.
- Mark D. Condon
- , Nicola J. Platt
- & Stephanie J. Cragg
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Article
| Open AccessA novel role for the actin-binding protein drebrin in regulating opiate addiction
The underlying transcriptional and cellular events mediating the reduction of dendritic spines on medium spiny neurons of the nucleus accumbens (NAc) remains unknown. Here, authors demonstrate that heroin self-administration negatively regulates the actin-binding protein drebrin in the NAc, which is shown to be transcriptionally repressed by the histone modifier HDAC2, and that overexpression of drebrin is sufficient to decrease drug seeking and increase dendritic spine density
- Jennifer A. Martin
- , Craig T. Werner
- & David M. Dietz
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Article
| Open AccessRole of laterodorsal tegmentum projections to nucleus accumbens in reward-related behaviors
The laterodorsal tegmental nucleus (LDT) is known to influence reward processing through its projections to the VTA. Here, the authors report that the cholinergic projections from the LDT to the nucleus accumbens play an important role in motivation and positive reinforcement behaviors.
- Bárbara Coimbra
- , Carina Soares-Cunha
- & Ana João Rodrigues
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Article
| Open AccessThe cost of obtaining rewards enhances the reward prediction error signal of midbrain dopamine neurons
Rewards that require high effort tend to be preferred over those that require low effort. Here, the authors show how the effort of obtaining rewards affects reward-related activity of dopamine neurons, and in turn the speed of learning stimulus-reward associations.
- Shingo Tanaka
- , John P. O’Doherty
- & Masamichi Sakagami
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Article
| Open AccessVentral midbrain stimulation induces perceptual learning and cortical plasticity in primates
Practice can improve the perception of stimuli used to achieve a task (perceptual learning). Here, the authors show in monkeys that perceptual learning can be produced even for irrelevant stimuli if the stimuli are paired with stimulation of a dopaminergic centre, the ventral tegmental area (VTA).
- John T. Arsenault
- & Wim Vanduffel
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| Open AccessFrom choice architecture to choice engineering
Qualitative psychological principles are commonly utilized to influence the choices that people make. Can this goal be achieved more efficiently by using quantitative models of choice? Here, we launch an academic competition to compare the effectiveness of these two approaches.
- Ohad Dan
- & Yonatan Loewenstein
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Article
| Open AccessThe neural computation of inconsistent choice behavior
Humans are often inconsistent when choosing between alternatives, but the neural basis of deviations from economic rationality is unclear. Here, the authors show that irrational choices arise in the same brain regions responsible for value computation, implying that brain ‘noise’ may underlie inconsistency.
- Vered Kurtz-David
- , Dotan Persitz
- & Dino J. Levy
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| Open AccessInactivation of a CRF-dependent amygdalofugal pathway reverses addiction-like behaviors in alcohol-dependent rats
Withdrawal from alcohol activates neurons in the central amygdala (CeA) and increases craving for alcohol. The authors show that these neurons predominantly express CRF and project to the BNST. Inactivation of this pathway reduces the dependence-related escalation of alcohol drinking.
- Giordano de Guglielmo
- , Marsida Kallupi
- & Olivier George