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1.
bioRxiv ; 2024 Jun 13.
Article in English | MEDLINE | ID: mdl-38915616

ABSTRACT

Noise is a fundamental problem for information processing in neural systems. In decision-making, noise is assumed to have a primary role in errors and stochastic choice behavior. However, little is known about how noise arising from different sources contributes to value coding and choice behaviors, especially when it interacts with neural computation. Here we examine how noise arising early versus late in the choice process differentially impacts context-dependent choice behavior. We found in model simulations that early and late noise predict opposing context effects: under early noise, contextual information enhances choice accuracy; while under late noise, context degrades choice accuracy. Furthermore, we verified these opposing predictions in experimental human choice behavior. Manipulating early and late noise - by inducing uncertainty in option values and controlling time pressure - produced dissociable positive and negative context effects. These findings reconcile controversial experimental findings in the literature reporting either context-driven impairments or improvements in choice performance, suggesting a unified mechanism for context-dependent choice. More broadly, these findings highlight how different sources of noise can interact with neural computations to differentially modulate behavior. Significance: The current study addresses the role of noise origin in decision-making, reconciling controversies around how decision-making is impacted by context. We demonstrate that different types of noise - either arising early during evaluation or late during option comparison - leads to distinct results: with early noise, context enhances choice accuracy, while with late noise, context impairs it. Understanding these dynamics offers potential strategies for improving decision-making in noisy environments and refining existing neural computation models. Overall, our findings advance our understanding of how neural systems handle noise in essential cognitive tasks, suggest a beneficial role for contextual modulation under certain conditions, and highlight the profound implications of noise structure in decision-making.

3.
Nat Commun ; 14(1): 7821, 2023 Nov 28.
Article in English | MEDLINE | ID: mdl-38016973

ABSTRACT

Evidence from monkeys and humans suggests that the orbitofrontal cortex (OFC) encodes the subjective value of options under consideration during choice. Data from non-human primates suggests that these value signals are context-dependent, representing subjective value in a way influenced by the decision makers' recent experience. Using electrodes distributed throughout cortical and subcortical structures, human epilepsy patients performed an auction task where they repeatedly reported the subjective values they placed on snack food items. High-gamma activity in many cortical and subcortical sites including the OFC positively correlated with subjective value. Other OFC sites showed signals contextually modulated by the subjective value of previously offered goods-a context dependency predicted by theory but not previously observed in humans. These results suggest that value and value-context signals are simultaneously present but separately represented in human frontal cortical activity.


Subject(s)
Choice Behavior , Frontal Lobe , Animals , Humans , Choice Behavior/physiology , Frontal Lobe/physiology , Prefrontal Cortex/physiology , Primates , Haplorhini , Decision Making , Reward
4.
Elife ; 122023 04 25.
Article in English | MEDLINE | ID: mdl-37096663

ABSTRACT

In value-based decision making, options are selected according to subjective values assigned by the individual to available goods and actions. Despite the importance of this faculty of the mind, the neural mechanisms of value assignments, and how choices are directed by them, remain obscure. To investigate this problem, we used a classic measure of utility maximization, the Generalized Axiom of Revealed Preference, to quantify internal consistency of food preferences in Caenorhabditis elegans, a nematode worm with a nervous system of only 302 neurons. Using a novel combination of microfluidics and electrophysiology, we found that C. elegans food choices fulfill the necessary and sufficient conditions for utility maximization, indicating that nematodes behave as if they maintain, and attempt to maximize, an underlying representation of subjective value. Food choices are well-fit by a utility function widely used to model human consumers. Moreover, as in many other animals, subjective values in C. elegans are learned, a process we find requires intact dopamine signaling. Differential responses of identified chemosensory neurons to foods with distinct growth potentials are amplified by prior consumption of these foods, suggesting that these neurons may be part of a value-assignment system. The demonstration of utility maximization in an organism with a very small nervous system sets a new lower bound on the computational requirements for utility maximization and offers the prospect of an essentially complete explanation of value-based decision making at single neuron resolution in this organism.


Subject(s)
Caenorhabditis elegans Proteins , Caenorhabditis elegans , Animals , Caenorhabditis elegans/physiology , Caenorhabditis elegans Proteins/metabolism , Food , Food Preferences , Signal Transduction
6.
Trends Cogn Sci ; 26(8): 669-687, 2022 08.
Article in English | MEDLINE | ID: mdl-35643845

ABSTRACT

For the past half-century, cognitive and social scientists have struggled with the irrationalities of human choice behavior; people consistently make choices that are logically inconsistent. Is human choice behavior evolutionarily adaptive or is it an inefficient patchwork of competing mechanisms? In this review, I present an interdisciplinary synthesis arguing for a novel interpretation: choice is efficiently irrational. Connecting findings across disciplines suggests that observed choice behavior reflects a precise optimization of the trade-off between the costs of increasing the precision of the choice mechanism and the declining benefits that come as precision increases. Under these constraints, a rationally imprecise strategy emerges that works toward optimal efficiency rather than toward optimal rationality. This approach rationalizes many of the puzzling inconsistencies of human choice behavior, explaining why these inconsistencies arise as an optimizing solution in biological choosers.


Subject(s)
Choice Behavior , Decision Making , Cognition , Humans
7.
Neuropsychopharmacology ; 47(8): 1440-1448, 2022 07.
Article in English | MEDLINE | ID: mdl-34916590

ABSTRACT

How does craving bias decisions to pursue drugs over other valuable, and healthier, alternatives in addiction? To address this question, we measured the in-the-moment economic decisions of people with opioid use disorder as they experienced craving, shortly after receiving their scheduled opioid maintenance medication and ~24 h later. We found that higher cravers had higher drug-related valuation, and that moments of higher craving within-person also led to higher drug-related valuation. When experiencing increased opioid craving, participants were willing to pay more for personalized consumer items and foods more closely related to their drug use, but not for alternative "nondrug-related" but equally desirable options. This selective increase in value with craving was greater when the drug-related options were offered in higher quantities and was separable from the effects of other fluctuating psychological states like negative mood. These findings suggest that craving narrows and focuses economic motivation toward the object of craving by selectively and multiplicatively amplifying perceived value along a "drug relatedness" dimension.


Subject(s)
Behavior, Addictive , Opioid-Related Disorders , Affect , Analgesics, Opioid/pharmacology , Craving , Humans , Opioid-Related Disorders/drug therapy
8.
Proc Natl Acad Sci U S A ; 118(35)2021 08 31.
Article in English | MEDLINE | ID: mdl-34446546

ABSTRACT

Since Odysseus committed to resisting the Sirens, mechanisms to limit self-control failure have been a central feature of human behavior. Psychologists have long argued that the use of self-control is an effortful process and, more recently, that its failure arises when the cognitive costs of self-control outweigh its perceived benefits. In a similar way, economists have argued that sophisticated choosers can adopt "precommitment strategies" that tie the hands of their future selves in order to reduce these costs. Yet, we still lack an empirical tool to quantify and demonstrate the cost of self-control. Here, we develop and validate an economic decision-making task to quantify the subjective cost of self-control by determining the monetary cost a person is willing to incur in order to eliminate the need for self-control. We find that humans will pay to avoid having to exert self-control in a way that scales with increasing levels of temptation and that these costs appear to be modulated both by motivational incentives and stress exposure. Our psychophysical approach allows us to index moment-to-moment self-control costs at the within-subject level, validating important theoretical work across multiple disciplines and opening avenues of self-control research in healthy and clinical populations.


Subject(s)
Costs and Cost Analysis , Health Care Costs , Self-Control , Adolescent , Adult , Cognition , Diet , Diet Therapy/economics , Female , Habits , Humans , Male , Middle Aged , Models, Psychological , Motivation , Stress, Psychological , Young Adult
10.
JAMA Psychiatry ; 77(4): 368-377, 2020 04 01.
Article in English | MEDLINE | ID: mdl-31812982

ABSTRACT

Importance: Opioid addiction is a major public health problem. Despite availability of evidence-based treatments, relapse and dropout are common outcomes. Efforts aimed at identifying reuse risk and gaining more precise understanding of the mechanisms conferring reuse vulnerability are needed. Objective: To use tools from computational psychiatry and decision neuroscience to identify changes in decision-making processes preceding opioid reuse. Design, Setting, and Participants: A cohort of individuals with opioid use disorder were studied longitudinally at a community-based treatment setting for up to 7 months (1-15 sessions per person). At each session, patients completed a risky decision-making task amenable to computational modeling and standard clinical assessments. Time-lagged mixed-effects logistic regression analyses were used to assess the likelihood of opioid use between sessions (t to t + 1; within the subsequent 1-4 weeks) from data acquired at the current session (t). A cohort of control participants completed similar procedures (1-5 sessions per person), serving both as a baseline comparison group and an independent sample in which to assess measurement test-retest reliability. Data were analyzed between January 1, 2018, and September 5, 2019. Main Outcomes and Measures: Two individual model-based behavioral markers were derived from the task completed at each session, capturing a participant's current tolerance of known risks and ambiguity (partially unknown risks). Current anxiety, craving, withdrawal, and nonadherence were assessed via interview and clinic records. Opioid use was ascertained from random urine toxicology tests and self-reports. Results: Seventy patients (mean [SE] age, 44.7 [1.3] years; 12 women and 58 men [82.9% male]) and 55 control participants (mean [SE] age, 42.4 [1.5] years; 13 women and 42 men [76.4% male]) were included. Of the 552 sessions completed with patients (mean [SE], 7.89 [0.59] sessions per person), 252 (45.7%) directly preceded opioid use events (mean [SE], 3.60 [0.44] sessions per person). From the task parameters, only ambiguity tolerance was significantly associated with increased odds of prospective opioid use (adjusted odds ratio, 1.37 [95% CI, 1.07-1.76]), indicating patients were more tolerant specifically of ambiguous risks prior to these use events. The association of ambiguity tolerance with prospective use was independent of established clinical factors (adjusted odds ratio, 1.29 [95% CI, 1.01-1.65]; P = .04), such that a model combining these factors explained more variance in reuse risk. No significant differences in ambiguity tolerance were observed between patients and control participants, who completed 197 sessions (mean [SE], 3.58 [0.21] sessions per person); however, patients were more tolerant of known risks (B = 0.56 [95% CI, 0.05-1.07]). Conclusions and Relevance: Computational approaches can provide mechanistic insights about the cognitive factors underlying opioid reuse vulnerability and may hold promise for clinical use.


Subject(s)
Decision Making , Opioid-Related Disorders/etiology , Risk-Taking , Adult , Case-Control Studies , Computer Simulation , Female , Humans , Longitudinal Studies , Male , Opioid-Related Disorders/psychology , Prospective Studies , Risk Factors , Time Factors , Uncertainty
11.
Philos Trans R Soc Lond B Biol Sci ; 374(1766): 20180135, 2019 02 18.
Article in English | MEDLINE | ID: mdl-30966919

ABSTRACT

Choice impulsivity is an important subcomponent of the broader construct of impulsivity and is a key feature of many psychiatric disorders. Choice impulsivity is typically quantified as temporal discounting, a well-documented phenomenon in which a reward's subjective value diminishes as the delay to its delivery is increased. However, an individual's proclivity to-or more commonly aversion to- risk can influence nearly all of the standard experimental tools available for measuring temporal discounting. Despite this interaction, risk preference is a behaviourally and neurobiologically distinct construct that relates to the economic notion of utility or subjective value. In this opinion piece, we discuss the mathematical relationship between risk preferences and time preferences, their neural implementation, and propose ways that research in psychiatry could, and perhaps should, aim to account for this relationship experimentally to better understand choice impulsivity and its clinical implications. This article is part of the theme issue 'Risk taking and impulsive behaviour: fundamental discoveries, theoretical perspectives and clinical implications'.


Subject(s)
Delay Discounting , Impulsive Behavior , Mental Disorders/psychology , Reward , Risk-Taking , Humans , Models, Psychological , Time Factors
12.
Nat Commun ; 9(1): 3206, 2018 08 10.
Article in English | MEDLINE | ID: mdl-30097577

ABSTRACT

Adaptation is a fundamental process crucial for the efficient coding of sensory information. Recent evidence suggests that similar coding principles operate in decision-related brain areas, where neural value coding adapts to recent reward history. However, the circuit mechanism for value adaptation is unknown, and the link between changes in adaptive value coding and choice behavior is unclear. Here we show that choice behavior in nonhuman primates varies with the statistics of recent rewards. Consistent with efficient coding theory, decision-making shows increased choice sensitivity in lower variance reward environments. Both the average adaptation effect and across-session variability are explained by a novel multiple timescale dynamical model of value representation implementing divisive normalization. The model predicts empirical variance-driven changes in behavior despite having no explicit knowledge of environmental statistics, suggesting that distributional characteristics can be captured by dynamic model architectures. These findings highlight the importance of treating decision-making as a dynamic process and the role of normalization as a unifying computation for contextual phenomena in choice.


Subject(s)
Adaptation, Psychological , Behavior, Animal/physiology , Choice Behavior/physiology , Animals , Macaca mulatta , Male , Models, Neurological , Reward , Task Performance and Analysis , Time Factors
13.
Proc Natl Acad Sci U S A ; 115(16): 4122-4127, 2018 04 17.
Article in English | MEDLINE | ID: mdl-29610355

ABSTRACT

Craving is thought to be a specific desire state that biases choice toward the desired object, be it chocolate or drugs. A vast majority of people report having experienced craving of some kind. In its pathological form craving contributes to health outcomes in addiction and obesity. Yet despite its ubiquity and clinical relevance we still lack a basic neurocomputational understanding of craving. Here, using an instantaneous measure of subjective valuation and selective cue exposure, we identify a behavioral signature of a food craving-like state and advance a computational framework for understanding how this state might transform valuation to bias choice. We find desire induced by exposure to a specific high-calorie, high-fat/sugar snack good is expressed in subjects' momentary willingness to pay for this good. This effect is selective but not exclusive to the exposed good; rather, we find it generalizes to nonexposed goods in proportion to their subjective attribute similarity to the exposed ones. A second manipulation of reward size (number of snack units available for purchase) further suggested that a multiplicative gain mechanism supports the transformation of valuation during laboratory craving. These findings help explain how real-world food craving can result in behaviors inconsistent with preferences expressed in the absence of craving and open a path for the computational modeling of craving-like phenomena using a simple and repeatable experimental tool for assessing subjective states in economic terms.


Subject(s)
Costs and Cost Analysis , Craving , Feeding Behavior/psychology , Models, Psychological , Snacks/psychology , Adolescent , Adult , Algorithms , Beverages/economics , Candy/economics , Choice Behavior , Cues , Fasting/psychology , Female , Food Preferences/psychology , Humans , Male , Mental Recall , Middle Aged , Models, Economic , Odorants , Photic Stimulation , Time Factors , Young Adult
14.
Nat Commun ; 9(1): 162, 2018 01 11.
Article in English | MEDLINE | ID: mdl-29323110

ABSTRACT

Normalization is a common cortical computation widely observed in sensory perception, but its importance in perception of reward value and decision making remains largely unknown. We examined (1) whether normalized value signals occur in the orbitofrontal cortex (OFC) and (2) whether changes in behavioral task context influence the normalized representation of value. We record medial OFC (mOFC) single neuron activity in awake-behaving monkeys during a reward-guided lottery task. mOFC neurons signal the relative values of options via a divisive normalization function when animals freely choose between alternatives. The normalization model, however, performed poorly in a variant of the task where only one of the two possible choice options yields a reward and the other was certain not to yield a reward (so called: "forced choice"). The existence of such context-specific value normalization may suggest that the mOFC contributes valuation signals critical for economic decision making when meaningful alternative options are available.


Subject(s)
Choice Behavior/physiology , Electrophysiology/methods , Models, Neurological , Prefrontal Cortex/physiology , Animals , Macaca mulatta , Neurons/physiology , Photic Stimulation , Prefrontal Cortex/diagnostic imaging , Reward
15.
PLoS One ; 13(1): e0191357, 2018.
Article in English | MEDLINE | ID: mdl-29373590

ABSTRACT

Measuring temporal discounting through the use of intertemporal choice tasks is now the gold standard method for quantifying human choice impulsivity (impatience) in neuroscience, psychology, behavioral economics, public health and computational psychiatry. A recent area of growing interest is individual differences in discounting levels, as these may predispose to (or protect from) mental health disorders, addictive behaviors, and other diseases. At the same time, more and more studies have been dedicated to the quantification of individual attitudes towards risk, which have been measured in many clinical and non-clinical populations using closely related techniques. Economists have pointed to interactions between measurements of time preferences and risk preferences that may distort estimations of the discount rate. However, although becoming standard practice in economics, discount rates and risk preferences are rarely measured simultaneously in the same subjects in other fields, and the magnitude of the imposed distortion is unknown in the assessment of individual differences. Here, we show that standard models of temporal discounting -such as a hyperbolic discounting model widely present in the literature which fails to account for risk attitudes in the estimation of discount rates- result in a large and systematic pattern of bias in estimated discounting parameters. This can lead to the spurious attribution of differences in impulsivity between individuals when in fact differences in risk attitudes account for observed behavioral differences. We advance a model which, when applied to standard choice tasks typically used in psychology and neuroscience, provides both a better fit to the data and successfully de-correlates risk and impulsivity parameters. This results in measures that are more accurate and thus of greater utility to the many fields interested in individual differences in impulsivity.


Subject(s)
Choice Behavior , Impulsive Behavior , Risk-Taking , Adult , Attitude , Female , Humans , Male , Middle Aged , Time Factors
16.
Proc Natl Acad Sci U S A ; 114(48): 12696-12701, 2017 11 28.
Article in English | MEDLINE | ID: mdl-29133418

ABSTRACT

The notion of subjective value is central to choice theories in ecology, economics, and psychology, serving as an integrated decision variable by which options are compared. Subjective value is often assumed to be an absolute quantity, determined in a static manner by the properties of an individual option. Recent neurobiological studies, however, have shown that neural value coding dynamically adapts to the statistics of the recent reward environment, introducing an intrinsic temporal context dependence into the neural representation of value. Whether valuation exhibits this kind of dynamic adaptation at the behavioral level is unknown. Here, we show that the valuation process in human subjects adapts to the history of previous values, with current valuations varying inversely with the average value of recently observed items. The dynamics of this adaptive valuation are captured by divisive normalization, linking these temporal context effects to spatial context effects in decision making as well as spatial and temporal context effects in perception. These findings suggest that adaptation is a universal feature of neural information processing and offer a unifying explanation for contextual phenomena in fields ranging from visual psychophysics to economic choice.


Subject(s)
Adaptation, Physiological , Choice Behavior/physiology , Cost-Benefit Analysis , Decision Making/physiology , Visual Perception/physiology , Adolescent , Adult , Female , Food , Humans , Male , Middle Aged , Reaction Time/physiology , Reward
17.
Soc Cogn Affect Neurosci ; 12(9): 1394-1401, 2017 09 01.
Article in English | MEDLINE | ID: mdl-28992268

ABSTRACT

In intertemporal choices between immediate and delayed rewards, people tend to prefer immediate rewards, often even when the delayed reward is larger. This is known as temporal discounting. It has been proposed that this tendency emerges because immediate rewards are more emotionally arousing than delayed rewards. However, in our previous research, we found no evidence for this but instead found that arousal responses (indexed with pupil dilation) in intertemporal choice are context-dependent. Specifically, arousal tracks the subjective value of the more variable reward option in the paradigm, whether it is immediate or delayed. Nevertheless, people tend to choose the less variable option in the choice task. In other words, their choices are reference-dependent and depend on variance in their recent history of offers. This suggests that there may be a causal relationship between reference-dependent choice and arousal, which we investigate here by reducing arousal pharmacologically using propranolol. Here, we show that propranolol reduces reference-dependence, leading to choices that are less influenced by recent history and more internally consistent.


Subject(s)
Adrenergic beta-Antagonists/pharmacology , Choice Behavior/drug effects , Propranolol/pharmacology , Adult , Arousal/drug effects , Delay Discounting/drug effects , Double-Blind Method , Female , Humans , Male , Psychomotor Performance/drug effects , Reflex, Pupillary/drug effects , Young Adult
18.
PLoS One ; 12(8): e0181112, 2017.
Article in English | MEDLINE | ID: mdl-28783734

ABSTRACT

Weather, in particular the intensity and duration of sunshine (luminance), has been shown to significantly affect financial markets. Yet, because of the complexity of market interactions we do not know how human behavior is affected by luminance in a way that could inform theoretical choice models. In this paper, we use data from a field study using an incentive-compatible, decision task conducted daily over a period of two years and from the US Earth System Research Laboratory luminance sensor to investigate the impact of luminance on risk preferences, ambiguity preferences, choice consistency and dominance violations. We find that luminance levels affect all of these. Age and gender influence the strength of some of these effects.


Subject(s)
Choice Behavior/radiation effects , Financial Management , Sunlight , Adult , Aged , Aged, 80 and over , Female , Humans , Male , Middle Aged , Motivation , Risk-Taking , Young Adult
19.
Nat Commun ; 7: 13822, 2016 12 13.
Article in English | MEDLINE | ID: mdl-27959326

ABSTRACT

Many decisions involve uncertainty, or 'risk', regarding potential outcomes, and substantial empirical evidence has demonstrated that human aging is associated with diminished tolerance for risky rewards. Grey matter volume in a region of right posterior parietal cortex (rPPC) is predictive of preferences for risky rewards in young adults, with less grey matter volume indicating decreased tolerance for risk. That grey matter loss in parietal regions is a part of healthy aging suggests that diminished rPPC grey matter volume may have a role in modulating risk preferences in older adults. Here we report evidence for this hypothesis and show that age-related declines in rPPC grey matter volume better account for age-related changes in risk preferences than does age per se. These results provide a basis for understanding the neural mechanisms that mediate risky choice and a glimpse into the neurodevelopmental dynamics that impact decision-making in an aging population.


Subject(s)
Decision Making , Gray Matter/pathology , Risk-Taking , Adolescent , Adult , Age Factors , Aged , Aged, 80 and over , Aging , Female , Gray Matter/anatomy & histology , Humans , Male , Middle Aged , Reward , Uncertainty
20.
J Neurosci Methods ; 270: 138-146, 2016 09 01.
Article in English | MEDLINE | ID: mdl-27339782

ABSTRACT

BACKGROUND: Video-based noninvasive eye trackers are an extremely useful tool for many areas of research. Many open-source eye trackers are available but current open-source systems are not designed to track eye movements with the temporal resolution required to investigate the mechanisms of oculomotor behavior. Commercial systems are available but employ closed source hardware and software and are relatively expensive, limiting wide-spread use. NEW METHOD: Here we present Oculomatic, an open-source software and modular hardware solution to eye tracking for use in humans and non-human primates. RESULTS: Oculomatic features high temporal resolution (up to 600Hz), real-time eye tracking with high spatial accuracy (<0.5°), and low system latency (∼1.8ms, 0.32ms STD) at a relatively low-cost. COMPARISON WITH EXISTING METHOD(S): Oculomatic compares favorably to our existing scleral search-coil system while being fully non invasive. CONCLUSIONS: We propose that Oculomatic can support a wide range of research into the properties and neural mechanisms of oculomotor behavior.


Subject(s)
Eye Movement Measurements/instrumentation , Algorithms , Animals , Equipment Failure , Eye Movements , Humans , Macaca mulatta , Male , Software , Time Factors
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