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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

Context-dependent choice and evaluation in real-world consumer behavior

Otto, A Ross; Devine, Sean; Schulz, Eric; Bornstein, Aaron M; Louie, Kenway
A body of work spanning neuroscience, economics, and psychology indicates that decision-making is context-dependent, which means that the value of an option depends not only on the option in question, but also on the other options in the choice set-or the 'context'. While context effects have been observed primarily in small-scale laboratory studies with tightly constrained, artificially constructed choice sets, it remains to be determined whether these context effects take hold in real-world choice problems, where choice sets are large and decisions driven by rich histories of direct experience. Here, we investigate whether valuations are context-dependent in real-world choice by analyzing a massive restaurant rating dataset as well as two independent replication datasets which provide complementary operationalizations of restaurant choice. We find that users make fewer ratings-maximizing choices in choice sets with higher-rated options-a hallmark of context-dependent choice-and that post-choice restaurant ratings also varied systematically with the ratings of unchosen restaurants. Furthermore, in a follow-up laboratory experiment using hypothetical choice sets matched to the real-world data, we find further support for the idea that subjective valuations of restaurants are scaled in accordance with the choice context, providing corroborating evidence for a general mechanistic-level account of these effects. Taken together, our results provide a potent demonstration of context-dependent choice in real-world choice settings, manifesting both in decisions and subjective valuation of options.
PMID: 36273073
ISSN: 2045-2322
CID: 5352602

Asymmetric and adaptive reward coding via normalized reinforcement learning

Louie, Kenway
Learning is widely modeled in psychology, neuroscience, and computer science by prediction error-guided reinforcement learning (RL) algorithms. While standard RL assumes linear reward functions, reward-related neural activity is a saturating, nonlinear function of reward; however, the computational and behavioral implications of nonlinear RL are unknown. Here, we show that nonlinear RL incorporating the canonical divisive normalization computation introduces an intrinsic and tunable asymmetry in prediction error coding. At the behavioral level, this asymmetry explains empirical variability in risk preferences typically attributed to asymmetric learning rates. At the neural level, diversity in asymmetries provides a computational mechanism for recently proposed theories of distributional RL, allowing the brain to learn the full probability distribution of future rewards. This behavioral and computational flexibility argues for an incorporation of biologically valid value functions in computational models of learning and decision-making.
PMID: 35862443
ISSN: 1553-7358
CID: 5279312

Excitatory-inhibitory tone shapes decision strategies in a hierarchical neural network model of multi-attribute choice

Pettine, Warren Woodrich; Louie, Kenway; Murray, John D; Wang, Xiao-Jing
We are constantly faced with decisions between alternatives defined by multiple attributes, necessitating an evaluation and integration of different information sources. Time-varying signals in multiple brain areas are implicated in decision-making; but we lack a rigorous biophysical description of how basic circuit properties, such as excitatory-inhibitory (E/I) tone and cascading nonlinearities, shape attribute processing and choice behavior. Furthermore, how such properties govern choice performance under varying levels of environmental uncertainty is unknown. We investigated two-attribute, two-alternative decision-making in a dynamical, cascading nonlinear neural network with three layers: an input layer encoding choice alternative attribute values; an intermediate layer of modules processing separate attributes; and a final layer producing the decision. Depending on intermediate layer E/I tone, the network displays distinct regimes characterized by linear (I), convex (II) or concave (III) choice indifference curves. In regimes I and II, each option's attribute information is additively integrated. In regime III, time-varying nonlinear operations amplify the separation between offer distributions by selectively attending to the attribute with the larger differences in input values. At low environmental uncertainty, a linear combination most consistently selects higher valued alternatives. However, at high environmental uncertainty, regime III is more likely than a linear operation to select alternatives with higher value. Furthermore, there are conditions where readout from the intermediate layer could be experimentally indistinguishable from the final layer. Finally, these principles are used to examine multi-attribute decisions in systems with reduced inhibitory tone, leading to predictions of different choice patterns and overall performance between those with restrictions on inhibitory tone and neurotypicals.
PMID: 33705386
ISSN: 1553-7358
CID: 4851972

The normalization of consumer valuations: Context-dependent preferences from neurobiological constraints

Webb, Ryan; Glimcher, Paul W.; Louie, Kenway
Consumer valuations are shaped by choice sets, exemplified by patterns of substitution between alternatives as choice sets are varied. Building on recent neuroeconomic evidence that valuations are transformed during the choice process, we incorporate the canonical divisive normalization computation into a discrete choice model and characterize how choice behaviour depends on both size and composition of the choice set. We then examine evidence for such behaviour from two choice experiments that vary the size and composition of the choice set. We find that divisive normalization more accurately captures observed behaviour than alternative models, including an example range normalization model. These results are robust across experimental paradigms. Finally, we demonstrate that Divisive Normalization implements an efficient means for the brain to represent valuations given neurobiological constraints, yielding the fewest choice errors possible given those constraints.
ISSN: 0025-1909
CID: 4769932

Divisive normalization does influence decisions with multiple alternatives [Letter]

Webb, Ryan; Glimcher, Paul W; Louie, Kenway
PMID: 32929203
ISSN: 2397-3374
CID: 4615582

Computational Markers of Risky Decision-making for Identification of Temporal Windows of Vulnerability to Opioid Use in a Real-world Clinical Setting

Konova, Anna B; Lopez-Guzman, Silvia; Urmanche, Adelya; Ross, Stephen; Louie, Kenway; Rotrosen, John; Glimcher, Paul W
Importance/UNASSIGNED: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/UNASSIGNED:To use tools from computational psychiatry and decision neuroscience to identify changes in decision-making processes preceding opioid reuse. Design, Setting, and Participants/UNASSIGNED: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/UNASSIGNED: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/UNASSIGNED: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/UNASSIGNED:Computational approaches can provide mechanistic insights about the cognitive factors underlying opioid reuse vulnerability and may hold promise for clinical use.
PMID: 31812982
ISSN: 2168-6238
CID: 4233972

Sensitivity of reaction time to the magnitude of rewards reveals the cost-structure of time

Steverson, Kai; Chung, Hui-Kuan; Zimmermann, Jan; Louie, Kenway; Glimcher, Paul
The Drift-Diffusion Model (DDM) is the prevalent computational model of the speed-accuracy trade-off in decision making. The DDM provides an explanation of behavior by optimally balancing reaction times and error rates. However, when applied to value-based decision making, the DDM makes the stark prediction that reaction times depend only on the relative utility difference between the options and not on absolute utility magnitudes. This prediction runs counter to evidence that reaction times decrease with higher utility magnitude. Here, we ask if and how it could be optimal for reaction times to show this observed pattern. We study an algorithmic framework that balances the cost of delaying rewards against the utility of obtained rewards. We find that the functional form of the cost of delay plays a key role, with the empirically observed pattern becoming optimal under multiplicative discounting. We add to the empirical literature by testing whether utility magnitude affects reaction times using a novel methodology that does not rely on functional form assumptions for the subjects' utilities. Our results advance the understanding of how and why reaction times are sensitive to the magnitude of rewards.
PMID: 31882745
ISSN: 2045-2322
CID: 4250982

Bounded rationality in C. elegans is explained by circuit-specific normalization in chemosensory pathways

Cohen, Dror; Teichman, Guy; Volovich, Meshi; Zeevi, Yoav; Elbaum, Lilach; Madar, Asaf; Louie, Kenway; Levy, Dino J; Rechavi, Oded
Rational choice theory assumes optimality in decision-making. Violations of a basic axiom of economic rationality known as "Independence of Irrelevant Alternatives" (IIA) have been demonstrated in both humans and animals and could stem from common neuronal constraints. Here we develop tests for IIA in the nematode Caenorhabditis elegans, an animal with only 302 neurons, using olfactory chemotaxis assays. We find that in most cases C. elegans make rational decisions. However, by probing multiple neuronal architectures using various choice sets, we show that violations of rationality arise when the circuit of olfactory sensory neurons is asymmetric. We further show that genetic manipulations of the asymmetry between the AWC neurons can make the worm irrational. Last, a context-dependent normalization-based model of value coding and gain control explains how particular neuronal constraints on information coding give rise to irrationality. Thus, we demonstrate that bounded rationality could arise due to basic neuronal constraints.
PMID: 31409788
ISSN: 2041-1723
CID: 4174942

Multiple timescales of normalized value coding underlie adaptive choice behavior

Zimmermann, Jan; Glimcher, Paul W; Louie, Kenway
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.
PMID: 30097577
ISSN: 2041-1723
CID: 3236552