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Publisher Correction: Electrophysiological population dynamics reveal context dependencies during decision making in human frontal cortex

Shih, Wan-Yu; Yu, Hsiang-Yu; Lee, Cheng-Chia; Chou, Chien-Chen; Chen, Chien; Glimcher, Paul W; Wu, Shih-Wei
PMID: 38102154
ISSN: 2041-1723
CID: 5589082

Electrophysiological population dynamics reveal context dependencies during decision making in human frontal cortex

Shih, Wan-Yu; Yu, Hsiang-Yu; Lee, Cheng-Chia; Chou, Chien-Chen; Chen, Chien; Glimcher, Paul W; Wu, Shih-Wei
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.
PMID: 38016973
ISSN: 2041-1723
CID: 5613522

Flexible control of representational dynamics in a disinhibition-based model of decision-making

Shen, Bo; Louie, Kenway; Glimcher, Paul
Inhibition is crucial for brain function, regulating network activity by balancing excitation and implementing gain control. Recent evidence suggests that beyond simply inhibiting excitatory activity, inhibitory neurons can also shape circuit function through disinhibition. While disinhibitory circuit motifs have been implicated in cognitive processes, including learning, attentional selection, and input gating, the role of disinhibition is largely unexplored in the study of decision-making. Here, we show that disinhibition provides a simple circuit motif for fast, dynamic control of network state and function. This dynamic control allows a disinhibition-based decision model to reproduce both value normalization and winner-take-all dynamics, the two central features of neurobiological decision-making captured in separate existing models with distinct circuit motifs. In addition, the disinhibition model exhibits flexible attractor dynamics consistent with different forms of persistent activity seen in working memory. Fitting the model to empirical data shows it captures well both the neurophysiological dynamics of value coding and psychometric choice behavior. Furthermore, the biological basis of disinhibition provides a simple mechanism for flexible top-down control of the network states, enabling the circuit to capture diverse task-dependent neural dynamics. These results suggest a biologically plausible unifying mechanism for decision-making and emphasize the importance of local disinhibition in neural processing.
PMID: 37261426
ISSN: 2050-084x
CID: 5538282

The nematode worm C. elegans chooses between bacterial foods as if maximizing economic utility

Katzen, Abraham; Chung, Hui-Kuan; Harbaugh, William T; Della Iacono, Christina; Jackson, Nicholas; Glater, Elizabeth E; Taylor, Charles J; Yu, Stephanie K; Flavell, Steven W; Glimcher, Paul W; Andreoni, James; Lockery, Shawn R
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.
PMID: 37096663
ISSN: 2050-084x
CID: 5507912

Expected subjective value theory (ESVT): A representation of decision under risk and certainty

Glimcher, Paul W.; Tymula, Agnieszka A.
We present a descriptive model of choice derived from neuroscientific models of efficient value representation in the brain. Our basic model, a special case of Expected Utility Theory, can capture a number of behaviors predicted by Prospect Theory. It achieves this with only two parameters: a time-indexed "payoff expectation" (reference point) and a free parameter we call "predisposition". A simple extension of the model outside the domain of Expected Utility also captures the Allais Paradox. Our models shed new light on the computational origins and evolution of risk attitudes and aversion to outcomes below reward expectation (reference point). It delivers novel explanations of the endowment effect, the observed heterogeneity in probability weighting functions, and the Allais Paradox, all with fewer parameters and higher descriptive accuracy than Prospect Theory.
ISSN: 0167-2681
CID: 5424042

Efficiently irrational: deciphering the riddle of human choice

Glimcher, Paul W
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.
PMID: 35643845
ISSN: 1879-307x
CID: 5277602

A neuroeconomic signature of opioid craving: How fluctuations in craving bias drug-related and nondrug-related value

Biernacki, Kathryn; Lopez-Guzman, Silvia; Messinger, John C; Banavar, Nidhi V; Rotrosen, John; Glimcher, Paul W; Konova, Anna B
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.
PMID: 34916590
ISSN: 1740-634x
CID: 5097792

P120. Cumulative Lifetime Stress is Selectively Associated With Ambiguity Aversion [Meeting Abstract]

Raio, C; Lu, B; Grubb, M; Shields, G; Slavich, G; Glimcher, P
Background: Stressor exposure is common in daily life where decisions involving uncertainty are made, yet the effects of stress on such decisions are equivocal across the literature. One reason for this is because research rarely dissociates between decisions involving risk (known outcome probabilities) and those involving ambiguity (unknown probabilities). Stress is thought to render appraisals of ambiguity more negative, but little work has examined if real-world stressor exposure differentially affect decisions involving risk vs. ambiguity.
Method(s): Across two studies, we used a comprehensive lifetime stressor inventory (Stress and Adversity Inventory for Adults) and a standard economic approach to quantify risk and ambiguity tolerance. Participants made 240 binary choices between a certain gain ($5) and a lottery option where they could win Result(s): In Study 1 (N=58), total stressor count and severity were each negatively correlated with the proportion of ambiguous lottery choices individuals were willing to accept (count: r=-0.33,p=0.01; severity: r=-0.39,p=0.002; Spearman's rho). In contrast, no relation emerged for risky choices (count: r=0.002,p=0.98; severity: r=-0.08,p=0.51). These ambiguity-selective effects were replicated in a second study (N=188) using regression analyses while controlling for age, gender, income and mental health (count: s=-0.25,SE=0.011,p=0.02; severity: s=-0.29,SE=0.011,p=0.01).
Conclusion(s): Participants experiencing greater lifetime stress were more averse to decisions involving ambiguity, but not risk. Our findings identify cumulative stressor exposure as a novel factor that is uniquely associated with a lower willingness to engage in explicit forms of decisions under uncertainty. Supported By: NIH Grant R01DA038063 (PWG) NIH Grant 5R01DA038063 (PWG) NIH Grant F32MH110135 (CMR) NIH Grant K08 MH103443 (GMS) NARSAD Young Investigator Grant (Brain and Behavior Foundation) (CMR) NARSAD Young Investigator Grant (Brain and Behavior Foundation) (GMS) Society in Science-Branco Weiss Fellowship (GMS) Keywords: Stress, Decision-Making, Ambiguity, Early Life Stress
ISSN: 1873-2402
CID: 5240282

Cumulative lifetime stressor exposure assessed by the STRAIN predicts economic ambiguity aversion

Raio, Candace M; B Lu, Benjamin; Grubb, Michael; Shields, Grant S; Slavich, George M; Glimcher, Paul
Uncertainty is inherent in most decisions humans make. Economists distinguish between two types of decision-making under non-certain conditions: those involving risk (i.e., known outcome probabilities) and those that involve ambiguity (i.e., unknown outcome probabilities). Prior research has identified individual differences that explain risk preferences, but little is known about factors associated with ambiguity aversion. Here, we hypothesized that cumulative exposure to major psychosocial stressors over the lifespan might be one factor that predicts individuals' ambiguity aversion. Across two studies (Study 1: n = 58, Mage = 25.7; Study 2: n = 188, Mage = 39.81), we used a comprehensive lifetime stressor exposure inventory (i.e., the Stress and Adversity Inventory for Adults, or STRAIN) and a standard economic approach to quantify risk and ambiguity preferences. Greater lifetime stressor exposure as measured by the STRAIN, particularly in early life, was associated with higher aversion to ambiguity but not risk preferences.
PMID: 35354811
ISSN: 2041-1723
CID: 5201222

Neither Threat of Shock nor Acute Psychosocial Stress Affects Ambiguity Attitudes

Sambrano, Deshawn Chatman; Lormestoire, Arlene; Raio, Candace; Glimcher, Paul; Phelps, Elizabeth A
Decisions under uncertainty can be differentiated into two classes: risky, which has known probabilistic outcomes, and ambiguous, which has unknown probabilistic outcomes. Across a variety of types of decisions, people find ambiguity extremely aversive, subjectively more aversive than risk. It has been shown that the transient sympathetic arousal response to a choice predicts decisions under ambiguity but not risk, and that lifetime stress uniquely predicts attitudes toward ambiguity. Building on these findings, this study explored whether we could bias ambiguity and risk preferences with an arousal or acute stress manipulation that is incidental to the choice in two independent experiments. One experiment induced sympathetic arousal with an anticipatory threat paradigm, and the other manipulated incidental acute stress via a psychosocial stressor. The efficacy of the manipulations was confirmed via pupil dilation and salivary cortisol, respectively. Participants made choices between a guaranteed $5 option and a lottery with either a known (risky) or unknown (ambiguous) probabilistic outcome. Consistent with previous findings, participants were more averse to a given level of ambiguity than to a numerically equal level of risk. However, in contrast to our hypothesis, we found no evidence that transient arousal or acute stress that is incidental to the choice biases ambiguity preferences.
PMID: 35791419
ISSN: 2662-205x
CID: 5280332