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  1. Article ; Online: Reliable population code for subjective economic value from heterogeneous neuronal signals in primate orbitofrontal cortex.

    Ferrari-Toniolo, Simone / Schultz, Wolfram

    Neuron

    2023  Volume 111, Issue 22, Page(s) 3683–3696.e7

    Abstract: Behavior-related neuronal signals often vary between neurons, which might reflect the unreliability of individual neurons or a truly heterogeneous code. This notion may also apply to economic ("value-based") choices and the underlying reward signals. ... ...

    Abstract Behavior-related neuronal signals often vary between neurons, which might reflect the unreliability of individual neurons or a truly heterogeneous code. This notion may also apply to economic ("value-based") choices and the underlying reward signals. Reward value is subjective and can be described by a nonlinearly weighted magnitude (utility) and probability. Defining subjective values relies on the continuity axiom, whose testing involves structured variations of a wide range of reward magnitudes and probabilities. Axiom compliance demonstrates understanding of the stimuli and the meaningful character of choices. Using these tests, we investigated the encoding of subjective economic value by neurons in a key economic-decision structure of the monkey brain, the orbitofrontal cortex (OFC). We found that individual neurons carry heterogeneous neuronal value signals that largely fail to match the animal's choices. However, neuronal population signals matched the animal's choices well, suggesting accurate subjective economic value encoding by a heterogeneous population of unreliable neurons.
    MeSH term(s) Animals ; Choice Behavior/physiology ; Prefrontal Cortex/physiology ; Neurons/physiology ; Behavior, Animal ; Reward ; Macaca mulatta
    Language English
    Publishing date 2023-09-06
    Publishing country United States
    Document type Journal Article ; Research Support, Non-U.S. Gov't
    ZDB-ID 808167-0
    ISSN 1097-4199 ; 0896-6273
    ISSN (online) 1097-4199
    ISSN 0896-6273
    DOI 10.1016/j.neuron.2023.08.009
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  2. Article ; Online: Recent advances in understanding the role of phasic dopamine activity.

    Schultz, Wolfram

    F1000Research

    2019  Volume 8

    Abstract: The latest animal neurophysiology has revealed that the dopamine reward prediction error signal drives neuronal learning in addition to behavioral learning and reflects subjective reward representations beyond explicit contingency. The signal complies ... ...

    Abstract The latest animal neurophysiology has revealed that the dopamine reward prediction error signal drives neuronal learning in addition to behavioral learning and reflects subjective reward representations beyond explicit contingency. The signal complies with formal economic concepts and functions in real-world consumer choice and social interaction. An early response component is influenced by physical impact, reward environment, and novelty but does not fully code prediction error. Some dopamine neurons are activated by aversive stimuli, which may reflect physical stimulus impact or true aversiveness, but they do not seem to code general negative value or aversive prediction error. The reward prediction error signal is complemented by distinct, heterogeneous, smaller and slower changes reflecting sensory and motor contributors to behavioral activation, such as substantial movement (as opposed to precise motor control), reward expectation, spatial choice, vigor, and motivation. The different dopamine signals seem to defy a simple unifying concept and should be distinguished to better understand phasic dopamine functions.
    MeSH term(s) Animals ; Dopamine/physiology ; Dopaminergic Neurons/physiology ; Learning ; Motivation ; Reward
    Chemical Substances Dopamine (VTD58H1Z2X)
    Language English
    Publishing date 2019-09-24
    Publishing country England
    Document type Journal Article ; Research Support, Non-U.S. Gov't ; Review
    ZDB-ID 2699932-8
    ISSN 2046-1402 ; 2046-1402
    ISSN (online) 2046-1402
    ISSN 2046-1402
    DOI 10.12688/f1000research.19793.1
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  3. Article ; Online: Recent advances in understanding the role of phasic dopamine activity [version 1; peer review

    Wolfram Schultz

    F1000Research, Vol

    3 approved]

    2019  Volume 8

    Abstract: The latest animal neurophysiology has revealed that the dopamine reward prediction error signal drives neuronal learning in addition to behavioral learning and reflects subjective reward representations beyond explicit contingency. The signal complies ... ...

    Abstract The latest animal neurophysiology has revealed that the dopamine reward prediction error signal drives neuronal learning in addition to behavioral learning and reflects subjective reward representations beyond explicit contingency. The signal complies with formal economic concepts and functions in real-world consumer choice and social interaction. An early response component is influenced by physical impact, reward environment, and novelty but does not fully code prediction error. Some dopamine neurons are activated by aversive stimuli, which may reflect physical stimulus impact or true aversiveness, but they do not seem to code general negative value or aversive prediction error. The reward prediction error signal is complemented by distinct, heterogeneous, smaller and slower changes reflecting sensory and motor contributors to behavioral activation, such as substantial movement (as opposed to precise motor control), reward expectation, spatial choice, vigor, and motivation. The different dopamine signals seem to defy a simple unifying concept and should be distinguished to better understand phasic dopamine functions.
    Keywords Medicine ; R ; Science ; Q
    Language English
    Publishing date 2019-09-01T00:00:00Z
    Publisher F1000 Research Ltd
    Document type Article ; Online
    Database BASE - Bielefeld Academic Search Engine (life sciences selection)

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  4. Article ; Online: Erratum to: Reward functions of the basal ganglia.

    Schultz, Wolfram

    Journal of neural transmission (Vienna, Austria : 1996)

    2017  Volume 124, Issue 9, Page(s) 1159

    Language English
    Publishing date 2017-06-26
    Publishing country Austria
    Document type Journal Article ; Published Erratum
    ZDB-ID 184163-4
    ISSN 1435-1463 ; 0300-9564
    ISSN (online) 1435-1463
    ISSN 0300-9564
    DOI 10.1007/s00702-017-1738-3
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  5. Article ; Online: Reward prediction error.

    Schultz, Wolfram

    Current biology : CB

    2017  Volume 27, Issue 10, Page(s) R369–R371

    Abstract: In this quick guide, Wolfram Schultz provides an introduction of reward prediction error, exploring ...

    Abstract In this quick guide, Wolfram Schultz provides an introduction of reward prediction error, exploring the signal of dopamine neurons and describing its potential role in reward accumulation, decision-making and everyday life.
    Language English
    Publishing date 2017-05-22
    Publishing country England
    Document type Journal Article
    ZDB-ID 1071731-6
    ISSN 1879-0445 ; 0960-9822
    ISSN (online) 1879-0445
    ISSN 0960-9822
    DOI 10.1016/j.cub.2017.02.064
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  6. Article ; Online: Worth the Work? Monkeys Discount Rewards by a Subjective Adapting Effort Cost.

    Burrell, Mark / Pastor-Bernier, Alexandre / Schultz, Wolfram

    The Journal of neuroscience : the official journal of the Society for Neuroscience

    2023  Volume 43, Issue 40, Page(s) 6796–6806

    Abstract: All life must solve how to allocate limited energy resources to maximize benefits from scarce opportunities. Economic theory posits decision makers optimize choice by maximizing the subjective benefit (utility) of reward minus the subjective cost ( ... ...

    Abstract All life must solve how to allocate limited energy resources to maximize benefits from scarce opportunities. Economic theory posits decision makers optimize choice by maximizing the subjective benefit (utility) of reward minus the subjective cost (disutility) of the required effort. While successful in many settings, this model does not fully account for how experience can alter reward-effort trade-offs. Here, we test how well the subtractive model of effort disutility explains the behavior of two male nonhuman primates (
    MeSH term(s) Animals ; Male ; Decision Making ; Choice Behavior ; Brain ; Learning ; Reward
    Language English
    Publishing date 2023-08-25
    Publishing country United States
    Document type Journal Article
    ZDB-ID 604637-x
    ISSN 1529-2401 ; 0270-6474
    ISSN (online) 1529-2401
    ISSN 0270-6474
    DOI 10.1523/JNEUROSCI.0115-23.2023
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  7. Article: Worth the work? Monkeys discount rewards by a subjective adapting effort cost.

    Burrell, Mark / Pastor-Bernier, Alexandre / Schultz, Wolfram

    bioRxiv : the preprint server for biology

    2023  

    Abstract: All life must solve how to allocate limited energy resources to maximise benefits from scarce opportunities. Economic theory posits decision makers optimise choice by maximising the subjective benefit (utility) of reward minus the subjective cost ( ... ...

    Abstract All life must solve how to allocate limited energy resources to maximise benefits from scarce opportunities. Economic theory posits decision makers optimise choice by maximising the subjective benefit (utility) of reward minus the subjective cost (disutility) of the required effort. While successful in many settings, this model does not fully account for how experience can alter reward-effort trade-offs. Here we test how well the subtractive model of effort disutility explains the behavior of two non-human primates (
    Significance: All decision-makers need to consider how much effort they need to expend when evaluating potential options. Economic theories suggest that the optimal way to choose is by cost-benefit analysis of reward against effort. To be able to do this efficiently over many decision contexts, this needs to be done flexibly, with appropriate adaptation to context and experience. Therefore, in aiming to understand how this might be achieved in the brain, it is important to first carefully measure the subjective cost of effort. Here we show monkeys make reward-effort cost-benefit decisions, subtracting the subjective cost of effort from the subjective value of rewards. Moreover, the subjective cost of effort is dependent on the monkeys’ experience of effort in previous trials.
    Language English
    Publishing date 2023-01-10
    Publishing country United States
    Document type Preprint
    DOI 10.1101/2023.01.10.523384
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  8. Article ; Online: Reward Value Revealed by Auction in Rhesus Monkeys.

    Al-Mohammad, Alaa / Schultz, Wolfram

    The Journal of neuroscience : the official journal of the Society for Neuroscience

    2021  Volume 42, Issue 8, Page(s) 1510–1528

    Abstract: Economic choice is thought to involve the elicitation of the subjective values of the choice options. Thus far, value estimation in animals has relied on stochastic choices between multiple options presented in repeated trials and expressed from averages ...

    Abstract Economic choice is thought to involve the elicitation of the subjective values of the choice options. Thus far, value estimation in animals has relied on stochastic choices between multiple options presented in repeated trials and expressed from averages of dozens of trials. However, subjective reward valuations are made moment-to-moment and do not always require alternative options; their consequences are usually felt immediately. Here, we describe a Becker-DeGroot-Marschak (BDM) auction-like mechanism that provides more direct and simple valuations with immediate consequences. The BDM encourages agents to truthfully reveal their true subjective value in individual choices ("incentive compatibility"). Male monkeys reliably placed well-ranked BDM bids for up to five juice volumes while paying from a water budget. The bids closely approximated the average subjective values estimated with conventional binary choices (BCs), thus demonstrating procedural invariance and aligning with the wealth of knowledge acquired with these less direct estimation methods. The feasibility of BDM bidding in monkeys paves the way for an analysis of subjective neuronal value signals in single trials rather than from averages; the feasibility also bridges the gap to the increasingly used BDM method in human neuroeconomics.
    MeSH term(s) Animals ; Choice Behavior/physiology ; Macaca mulatta ; Male ; Neurons/physiology ; Reward
    Language English
    Publishing date 2021-12-22
    Publishing country United States
    Document type Journal Article ; Research Support, Non-U.S. Gov't
    ZDB-ID 604637-x
    ISSN 1529-2401 ; 0270-6474
    ISSN (online) 1529-2401
    ISSN 0270-6474
    DOI 10.1523/JNEUROSCI.1275-21.2021
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  9. Article ; Online: Functions of primate amygdala neurons in economic decisions and social decision simulation.

    Grabenhorst, Fabian / Schultz, Wolfram

    Behavioural brain research

    2021  Volume 409, Page(s) 113318

    Abstract: Long implicated in aversive processing, the amygdala is now recognized as a key component of the brain systems that process rewards. Beyond reward valuation, recent findings from single-neuron recordings in monkeys indicate that primate amygdala neurons ... ...

    Abstract Long implicated in aversive processing, the amygdala is now recognized as a key component of the brain systems that process rewards. Beyond reward valuation, recent findings from single-neuron recordings in monkeys indicate that primate amygdala neurons also play an important role in decision-making. The reward value signals encoded by amygdala neurons constitute suitable inputs to economic decision processes by being sensitive to reward contingency, relative reward quantity and temporal reward structure. During reward-based decisions, individual amygdala neurons encode both the value inputs and corresponding choice outputs of economic decision processes. The presence of such value-to-choice transitions in single amygdala neurons, together with other well-defined signatures of decision computation, indicate that a decision mechanism may be implemented locally within the primate amygdala. During social observation, specific amygdala neurons spontaneously encode these decision signatures to predict the choices of social partners, suggesting neural simulation of the partner's decision-making. The activity of these 'simulation neurons' could arise naturally from convergence between value neurons and social, self-other discriminating neurons. These findings identify single-neuron building blocks and computational architectures for decision-making and social behavior in the primate amygdala. An emerging understanding of the decision function of primate amygdala neurons can help identify potential vulnerabilities for amygdala dysfunction in human conditions afflicting social cognition and mental health.
    MeSH term(s) Amygdala/physiology ; Animals ; Behavior, Animal/physiology ; Decision Making/physiology ; Neurons/physiology ; Primates/physiology ; Reward ; Social Behavior ; Social Cognition
    Language English
    Publishing date 2021-04-24
    Publishing country Netherlands
    Document type Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Review
    ZDB-ID 449927-x
    ISSN 1872-7549 ; 0166-4328
    ISSN (online) 1872-7549
    ISSN 0166-4328
    DOI 10.1016/j.bbr.2021.113318
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  10. Article: Risky choice: Probability weighting explains independence axiom violations in monkeys.

    Ferrari-Toniolo, Simone / Seak, Leo Chi U / Schultz, Wolfram

    Journal of risk and uncertainty

    2022  Volume 65, Issue 3, Page(s) 319–351

    Abstract: Expected Utility Theory (EUT) provides axioms for maximizing utility in risky choice. The Independence Axiom (IA) is its most demanding axiom: preferences between two options should not change when altering both options equally by mixing them with a ... ...

    Abstract Expected Utility Theory (EUT) provides axioms for maximizing utility in risky choice. The Independence Axiom (IA) is its most demanding axiom: preferences between two options should not change when altering both options equally by mixing them with a common gamble. We tested common consequence (CC) and common ratio (CR) violations of the IA over several months in thousands of stochastic choices using a large variety of binary option sets. Three monkeys showed consistently few outright
    Supplementary information: The online version contains supplementary material available at 10.1007/s11166-022-09388-7.
    Language English
    Publishing date 2022-07-22
    Publishing country United States
    Document type Journal Article
    ZDB-ID 1478894-9
    ISSN 1573-0476 ; 0895-5646
    ISSN (online) 1573-0476
    ISSN 0895-5646
    DOI 10.1007/s11166-022-09388-7
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