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| Open AccessOptogenetic manipulation of a value-coding pathway from the primate caudate tail facilitates saccadic gaze shift
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.
- Hidetoshi Amita
- , Hyoung F. Kim
- & Okihide Hikosaka
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Article
| Open AccessResponse outcomes gate the impact of expectations on perceptual decisions
The authors use a combination of perceptual decision making in rats and computational modeling to explore the interplay of priors and sensory cues. They find that rats can learn to either alternate or repeat their actions based on reward likelihood and the influence of bias on their actions disappears after making an error.
- Ainhoa Hermoso-Mendizabal
- , Alexandre Hyafil
- & Jaime de la Rocha
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Article
| Open AccessTask complexity interacts with state-space uncertainty in the arbitration between model-based and model-free learning
The brain dynamically arbitrates between two model-based and model-free reinforcement learning (RL). Here, the authors show that participants tended to increase model-based control in response to increasing task complexity, but resorted to model-free when both uncertainty and task complexity were high.
- Dongjae Kim
- , Geon Yeong Park
- & Sang Wan Lee
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Article
| Open AccessHuman confidence judgments reflect reliability-based hierarchical integration of contextual information
Because our immediate observations are often ambiguous, we must use the context (prior beliefs) to guide inference, but the context may also be uncertain. Here, the authors show that humans can accurately estimate the reliability of the context and combine it with sensory uncertainty to form their decisions and estimate confidence.
- Philipp Schustek
- , Alexandre Hyafil
- & Rubén Moreno-Bote
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Article
| 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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Article
| 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 AccessContributions of anterior cingulate cortex and basolateral amygdala to decision confidence and learning under uncertainty
The degree of subjective confidence in deciding based on ambiguous sensory cues facilitates learning. Here, the authors report distinct functions of the basolateral amygdala and anterior cingulate cortex on implicit confidence judgements as well as flexible learning under uncertain conditions in rats.
- A. Stolyarova
- , M. Rakhshan
- & A. Izquierdo
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Article
| Open AccessPupil-linked phasic arousal evoked by violation but not emergence of regularity within rapid sound sequences
The neurotransmitter Norepinephrine (NE) has been implicated in coding surprise during decision making. Here, the authors demonstrate that this extends to sensory processing: NE release is specific to unexpected events even on extremely rapid time scales and without explicit tracking of probability.
- Sijia Zhao
- , Maria Chait
- & Hsin-I Liao
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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 AccessBounded rationality in C. elegans is explained by circuit-specific normalization in chemosensory pathways
Innate odor preferences in C. elegans are controlled by the activation of a pair of olfactory sensory neurons. Here, the authors show that asymmetric activation of the AWCON and AWCOFF neurons can lead to irrational olfactory preferences that are explained by a model of normalization of sensory gain control.
- Dror Cohen
- , Guy Teichman
- & Oded Rechavi
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Article
| Open AccessIrrational behavior in C. elegans arises from asymmetric modulatory effects within single sensory neurons
C. elegans worms exhibit an innate preference for various stimuli. Here the authors test the pairwise behavioral preference between a large set of stimuli and report that the worms’ behavior does not conform to rationality theory due to asymmetric modulatory effects within single sensory neurons.
- Shachar Iwanir
- , Rotem Ruach
- & Alon Zaslaver
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Article
| Open AccessCerebellar disruption impairs working memory during evidence accumulation
Disruption of cerebellar activity impairs working memory during evidence accumulation in mice. Here, the authors show that optogenetic perturbation of Purkinje cell activity disrupts the accurate accumulation of somatosensory information in working memory during perceptual decision-making.
- Ben Deverett
- , Mikhail Kislin
- & Samuel S.-H. Wang
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Article
| Open AccessA neural circuit model of decision uncertainty and change-of-mind
We make decisions with varying degrees of confidence and, if our confidence in a decision falls, we may change our mind. Here, the authors present a neuronal circuit model to account for how change of mind occurs under particular low-confidence conditions.
- Nadim A. A. Atiya
- , Iñaki Rañó
- & KongFatt Wong-Lin
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Article
| Open AccessDissociating task acquisition from expression during learning reveals latent knowledge
Performance is generally used as a metric to assay whether an animal has learnt a particular perceptual task. Here the authors demonstrate that in the context of probe trials without the possibility of reward, animals perform the correct instrumental response suggesting a latent knowledge of the task much before it is manifest in their performance.
- Kishore V. Kuchibhotla
- , Tom Hindmarsh Sten
- & Robert C. Froemke
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Article
| Open AccessMacaque dorsal premotor cortex exhibits decision-related activity only when specific stimulus–response associations are known
It is not clear to what degree activity in dorsal premotor cortex (PMd) reflects perceptual-deliberation versus action-selection aspects of decision-making. Here, the authors report that monkey PMd neurons do not express correlates of the perceptual decision independently of the action choices.
- Megan Wang
- , Christéva Montanède
- & John F. Kalaska
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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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Article
| Open AccessThe computational and neural substrates of moral strategies in social decision-making
The authors show that individuals apply different ‘moral strategies’ in interpersonal decision-making. These strategies are linked to distinct patterns of neural activity, even when they produce the same choice outcomes, illuminating how distinct moral principles can guide social behavior.
- Jeroen M. van Baar
- , Luke J. Chang
- & Alan G. Sanfey
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Article
| Open AccessDeviation from the matching law reflects an optimal strategy involving learning over multiple timescales
Recent experience can only provide limited information to guide decisions in a volatile environment. Here, the authors report that the choices made by a monkey in a dynamic foraging task can be better explained by a model that combines learning on both fast and slow timescales.
- Kiyohito Iigaya
- , Yashar Ahmadian
- & Stefano Fusi
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Article
| Open AccessEvidence for model-based encoding of Pavlovian contingencies in the human brain
Pavlovian conditioning involves model-free learning that associates predictive stimuli with their outcome value. Here, the authors present evidence for activation of OFC and striatum that is consistent with model based information during a pavlovian task with multiple stimuli that predict rewards.
- Wolfgang M. Pauli
- , Giovanni Gentile
- & John P. O’Doherty
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| Open AccessRetrospective model-based inference guides model-free credit assignment
The reinforcement learning literature suggests decisions are based on a model-free system, operating retrospectively, and a model-based system, operating prospectively. Here, the authors show that a model-based retrospective inference of a reward’s cause, guides model-free credit-assignment.
- Rani Moran
- , Mehdi Keramati
- & Raymond J. Dolan
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| Open AccessNeuronal evidence for good-based economic decisions under variable action costs
Choices between goods often depend on the action costs, but the mechanisms underlying economic decisions under variable action cost are poorly understood. Here, the authors record from neurons in the monkey orbitofrontal cortex and show that decisions under variable action cost were made in a non-spatial representation.
- Xinying Cai
- & Camillo Padoa-Schioppa
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Article
| Open AccessPrefrontal mechanisms combining rewards and beliefs in human decision-making
Optimal decision-making requires integrating expectations about rewards with beliefs about reward contingencies. Here, the authors show that these aspects of reward are encoded in the ventromedial prefrontal cortex then combined in the dorsomedial prefrontal cortex, a process that guides choice biases characteristic of human decision-making.
- Marion Rouault
- , Jan Drugowitsch
- & Etienne Koechlin
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| Open AccessAn orderly single-trial organization of population dynamics in premotor cortex predicts behavioral variability
To explain the neural correlates of behavior and its variability, one must analyze single-trial population dynamics. Here, the authors develop a statistical method that extracts low-dimensional dynamics that explain behavior better than high-dimensional neural activity revealing unexpected structure.
- Ziqiang Wei
- , Hidehiko Inagaki
- & Shaul Druckmann
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Article
| Open AccessCortical beta power reflects decision dynamics and uncovers multiple facets of post-error adaptation
People slow down reactions after errors, yet it is debated whether the mechanisms behind this slowing are beneficial for future performance. Here, the authors show that EEG measures converge with model predictions supporting a complex but overall beneficial mechanism of post-error slowing.
- Adrian G. Fischer
- , Roland Nigbur
- & Markus Ullsperger
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Article
| Open AccessSound identity is represented robustly in auditory cortex during perceptual constancy
Perceptual constancy requires neural representations selective for object identity, yet tolerant of identity-preserving transformations. Here, the authors show that sound identity is represented robustly in auditory cortex and that behavioral generalization requires precise timing of identity information.
- Stephen M. Town
- , Katherine C. Wood
- & Jennifer K. Bizley
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Article
| Open AccessNeural mechanisms for learning self and other ownership
The sense of ownership – of which objects belong to us and which to others - is an important part of our lives, but how the brain keeps track of ownership is poorly understood. Here, the authors show that specific brain areas are involved in ownership acquisition for the self, friends, and strangers.
- Patricia L. Lockwood
- , Marco K. Wittmann
- & Matthew F. S. Rushworth
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Article
| Open AccessLate Bayesian inference in mental transformations
Humans compensate for sensory noise by biasing sensory estimates toward prior expectations, as predicted by models of Bayesian inference. Here, the authors show that humans perform ‘late inference’ downstream of sensory processing to mitigate the effects of noisy internal mental computations.
- Evan D. Remington
- , Tiffany V. Parks
- & Mehrdad Jazayeri
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Article
| Open AccessRats adopt the optimal timescale for evidence integration in a dynamic environment
In a dynamic environment old evidence could be outdated. Here, the authors investigate the ability of rats to integrate and discount evidence provided by auditory clicks to infer a hidden, dynamic, state of the world and model the consequence of sensory noise to explain the source of errors.
- Alex T. Piet
- , Ahmed El Hady
- & Carlos D. Brody
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Article
| Open AccessDecisions are expedited through multiple neural adjustments spanning the sensorimotor hierarchy
When needed, we can speed up our decisions at the expense of accuracy. Here, the authors employ a novel human electrophysiology paradigm to show that hastened decisions are implemented through multiple, fundamentally distinct neural process adjustments across the sensorimotor hierarchy.
- Natalie A. Steinemann
- , Redmond G. O’Connell
- & Simon P. Kelly
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Article
| Open AccessBiased sequential sampling underlies the effects of time pressure and delay in social decision making
It has been proposed that humans make unselfish decisions if constrained to decide quickly, but other research has suggested that time constraint makes us selfish. Here, the authors reconcile these two views showing that pro-social people become more pro-social under time pressure, but selfish subjects do the opposite.
- Fadong Chen
- & Ian Krajbich
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Article
| Open AccessSaccade metrics reflect decision-making dynamics during urgent choices
Saccades have been extensively used to report choices in perceptual decision making studies yet little is known about the influence of covert decision-related processes on saccade metrics. Here, the authors demonstrate that saccade kinematics is a reliable tell about the degree of decision certainty.
- Joshua A. Seideman
- , Terrence R. Stanford
- & Emilio Salinas
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Article
| Open AccessInfralimbic cortex is required for learning alternatives to prelimbic promoted associations through reciprocal connectivity
Prelimbic (PL) and infralimbic (IL) cortical areas are known to have complementary roles in learning and decision making. Here the authors report reciprocal connectivity between the two areas and elucidate their functional impact on different aspects of learning.
- Arghya Mukherjee
- & Pico Caroni
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Article
| Open AccessTask-dependent representations of stimulus and choice in mouse parietal cortex
The precise role of PPC in transforming sensory signals to relevant actions is not yet clear. Here, the authors show that unlike V1, which is largely driven by visual input, PPC is strongly task-dependent and exhibits a mixture of stimulus and choice signals in a visual decision task.
- Gerald N. Pho
- , Michael J. Goard
- & Mriganka Sur
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| Open AccessDissociable neural mechanisms track evidence accumulation for selection of attention versus action
Decision-making involves parallel information processing regarding what stimulus dimension to pay attention to and what action to take. Here, the authors show that vmPFC tracks the value of the attended attribute while dACC tracks the degree to which it is attended.
- Amitai Shenhav
- , Mark A. Straccia
- & Matthew M. Botvinick
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Article
| Open AccessReward probability and timing uncertainty alter the effect of dorsal raphe serotonin neurons on patience
Activation of serotonin neurons in the dorsal raphe nucleus promotes patience in waiting for future rewards. Here the authors show that this effect is maximal for high probability reward or high temporal reward uncertainty suggesting that it boosts the prior probability of reward.
- Katsuhiko Miyazaki
- , Kayoko W. Miyazaki
- & Kenji Doya
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Article
| Open AccessNeuro-computational account of how mood fluctuations arise and affect decision making
Fluctuations in mood are known to affect our decisions. Here the authors propose and validate a model of how mood fluctuations arise through a slow integration of positive and negative feedback and report the resulting key changes in brain activity that modulate our decision making.
- Fabien Vinckier
- , Lionel Rigoux
- & Mathias Pessiglione
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| Open AccessIdentity prediction errors in the human midbrain update reward-identity expectations in the orbitofrontal cortex
Responses in the dopaminergic midbrain are known to signal prediction errors for reward value. Here, the authors show that the human midbrain also encodes errors in predicted reward identity, and that these signals update expectations of reward identity in the orbitofrontal cortex.
- James D. Howard
- & Thorsten Kahnt
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Article
| Open AccessStable representation of sounds in the posterior striatum during flexible auditory decisions
Striatum mediates goal-oriented behaviors and habitual actions. This study shows that auditory information is represented by neuronal activity of the posterior tail of the dorsal striatum in mice, and that this brain region mediates rodent’s flexible decision making based on auditory cues.
- Lan Guo
- , William I. Walker
- & Santiago Jaramillo
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Article
| Open AccessNeural basis for categorical boundaries in the primate pre-SMA during relative categorization of time intervals
Grouping stimuli into categories often depends on a subjective determination of category boundaries. Here the authors report a neuronal population in pre-supplementary motor area whose peak activity predicts the categorical decision boundary between long and short time intervals on a trial-by-trial basis.
- Germán Mendoza
- , Juan Carlos Méndez
- & Hugo Merchant
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| Open AccessHeuristic and optimal policy computations in the human brain during sequential decision-making
Alhough humans often make a series of related decisions, it is unknown whether this is done by relying on optimal or heuristic strategies. Here, the authors show that humans rely on both the best heuristic and the optimal policy, and that these strategies are controlled by parts of the medial prefrontal cortex.
- Christoph W. Korn
- & Dominik R. Bach
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Article
| Open AccessFree choice shapes normalized value signals in medial orbitofrontal cortex
Neurons in prefrontal areas including the medial orbitofrontal cortex (mOFC) represent the relative reward value of choices. Here the authors report that mOFC neurons implement divisive normalization to encode the relative values of lottery options only when the decision involves free choice.
- Hiroshi Yamada
- , Kenway Louie
- & Paul W. Glimcher
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Article
| Open AccessNeural computations underpinning the strategic management of influence in advice giving
Though it's important to influence others' decisions, the neural correlates of persuasive strategies are not known. Here, authors show that people change their advice based on its accuracy and whether they are being listened to, and identify the distinct brain regions underpinning each strategy.
- Uri Hertz
- , Stefano Palminteri
- & Bahador Bahrami
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Article
| Open AccessSimultaneous representation of a spectrum of dynamically changing value estimates during decision making
Activity in dorsal anterior cingulate cortex (dACC) dynamically tracks the value of the choice after every outcome. Here the authors report that dACC represents topographic maps of value estimates for different learning rates and interacts with similar maps in other areas at the time of the decision.
- David Meder
- , Nils Kolling
- & Matthew F.S. Rushworth
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Article
| Open AccessDistributed neural representation of saliency controlled value and category during anticipation of rewards and punishments
Stimulus category, saliency and value all affect the subjective value estimates that guide our decisions. Here, the authors systematically vary their stimuli along these three dimensions in humans and report category independent encoding of values and saliency in the vmPFC and striatum.
- Zhihao Zhang
- , Jennifer Fanning
- & Ifat Levy
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Article
| Open AccessInverted activity patterns in ventromedial prefrontal cortex during value-guided decision-making in a less-is-more task
Ventromedial prefrontal cortex in humans shows functional magnetic resonance imaging signals related to the subjective values of choices that are taken during decision-making as well as task-negative signals. Here, the authors report that in macaque ventromedial prefrontal cortex both activity patterns are inverted and lesions of this area disrupt subjective choice evaluation.
- Georgios K. Papageorgiou
- , Jerome Sallet
- & Matthew F. S. Rushworth
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Article
| Open AccessFeature-based learning improves adaptability without compromising precision
Learning about a rewarded outcome is complicated by the fact that a choice often incorporates multiple features with differing association with the reward. Here the authors demonstrate that feature-based learning is an efficient and adaptive strategy in dynamically changing environments.
- Shiva Farashahi
- , Katherine Rowe
- & Alireza Soltani
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Article
| Open AccessShort-term reward experience biases inference despite dissociable neural correlates
Making a good decision often requires the weighing of relative short-term rewards against long-term benefits, yet how the brain does this is not understood. Here, authors show that long-term beliefs are biased by reward experience and that dissociable brain regions facilitate both types of learning.
- Adrian G. Fischer
- , Sacha Bourgeois-Gironde
- & Markus Ullsperger
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Article
| Open AccessHistory-based action selection bias in posterior parietal cortex
Past outcomes modulate activity in a diverse set of brain regions however their precise influence on decisions is not known. Here the authors show that posterior parietal cortex neurons encode history-related signals between trials and optogenetic inactivation during this epoch disrupts the history dependence of choice.
- Eun Jung Hwang
- , Jeffrey E. Dahlen
- & Takaki Komiyama
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Article
| Open AccessDecoupled choice-driven and stimulus-related activity in parietal neurons may be misrepresented by choice probabilities
Choice-related signals in neuronal activity may reflect bottom-up sensory processes, top-down decision-related influences, or a combination of the two. Here the authors report that choice-related activity in VIP neurons is not predictable from their stimulus tuning, and that dominant choice signals can bias the standard metric of choice preference (choice probability).
- Adam Zaidel
- , Gregory C. DeAngelis
- & Dora E. Angelaki