The Representation of Decision Variables in Orbitofrontal Cortex is Longitudinally Stable.

The computation and comparison of subjective values underlying economic choices rely on the orbitofrontal cortex (OFC). In this area, distinct groups of neurons encode the value of individual options, the binary choice outcome, and the chosen value. These variables capture both the input and the output of the choice process, suggesting that the cell groups found in OFC constitute the building blocks of a decision circuit. Here we show that this neural circuit is longitudinally stable. Using two-photon calcium imaging, we recorded from mice choosing between different juice flavors. Recordings of individual cells continued for up to 20 weeks. For each cell and each pair of sessions, we compared the activity profiles using cosine similarity, and we assessed whether the cell encoded the same variable in both sessions. These analyses revealed a high degree of stability and a modest representational drift. A quantitative estimate indicated this drift would not randomize the circuit within the animal's lifetime.

Orbitofrontal cortex contributes to the comparison of values underlying economic choices.

Economic choices between goods entail the computation and comparison of subjective values. Previous studies examined neuronal activity in the orbitofrontal cortex (OFC) of monkeys choosing between different types of juices. Three groups of neurons were identified: offer value cells encoding the value of individual offers, chosen juice cells encoding the identity of the chosen juice, and chosen value cells encoding the value of the chosen offer. The encoded variables capture both the input (offer value) and the output (chosen juice, chosen value) of the decision process, suggesting that values are compared within OFC. Recent work demonstrates that choices are causally linked to the activity of offer value cells. Conversely, the hypothesis that OFC contributes to value comparison has not been confirmed. Here we show that weak electrical stimulation of OFC specifically disrupts value comparison without altering offer values. This result implies that neuronal populations in OFC participate in value comparison.

Neuronal origins of reduced accuracy and biases in economic choices under sequential offers.

Economic choices are characterized by a variety of biases. Understanding their origins is a long-term goal for neuroeconomics, but progress on this front has been limited. Here, we examined choice biases observed when two goods are offered sequentially. In the experiments, rhesus monkeys chose between different juices offered simultaneously or in sequence. Choices under sequential offers were less accurate (higher variability). They were also biased in favor of the second offer (order bias) and in favor of the preferred juice (preference bias). Analysis of neuronal activity recorded in the orbitofrontal cortex revealed that these phenomena emerged at different computational stages. Lower choice accuracy reflected weaker offer value signals (valuation stage), the order bias emerged during value comparison (decision stage), and the preference bias emerged late in the trial (post-comparison). By neuronal measures, each phenomenon reduced the value obtained on average in each trial and was thus costly to the monkey.

Logistic analysis of choice data: A primer.

Logistic regressions were developed in economics to model individual choice behavior. In recent years, they have become an important tool in decision neuroscience. Here, I describe and discuss different logistic models, emphasizing the underlying assumptions and possible interpretations. Logistic models may be used to quantify a variety of behavioral traits, including the relative subjective value of different goods, the choice accuracy, risk attitudes, and choice biases. More complex logistic models can be used for choices between good bundles, in cases of nonlinear value functions, and for choices between multiple options. Finally, logistic models can quantify the explanatory power of neuronal activity on choices, thus providing a valid alternative to receiver operating characteristic (ROC) analyses.

Economic Choices under Simultaneous or Sequential Offers Rely on the Same Neural Circuit.

A series of studies in which monkeys chose between two juices offered in variable amounts identified in the orbitofrontal cortex (OFC) different groups of neurons encoding the value of individual options (offer value), the binary choice outcome (chosen juice), and the chosen value. These variables capture both the input and the output of the choice process, suggesting that the cell groups identified in OFC constitute the building blocks of a decision circuit. Several lines of evidence support this hypothesis. However, in previous experiments offers were presented simultaneously, raising the question of whether current notions generalize to when goods are presented or are examined in sequence. Recently, Ballesta and Padoa-Schioppa (2019) examined OFC activity under sequential offers. An analysis of neuronal responses across time windows revealed that a small number of cell groups encoded specific sequences of variables. These sequences appeared analogous to the variables identified under simultaneous offers, but the correspondence remained tentative. Thus, in the present study, we examined the relation between cell groups found under sequential versus simultaneous offers. We recorded from the OFC while monkeys chose between different juices. Trials with simultaneous and sequential offers were randomly interleaved in each session. We classified cells in each choice modality, and we examined the relation between the two classifications. We found a strong correspondence; in other words, the cell groups measured under simultaneous offers and under sequential offers were one and the same. This result indicates that economic choices under simultaneous or sequential offers rely on the same neural circuit.SIGNIFICANCE STATEMENT Research in the past 20 years has shed light on the neuronal underpinnings of economic choices. A large number of results indicates that decisions between goods are formed in a neural circuit within the orbitofrontal cortex. In most previous studies, subjects chose between two goods offered simultaneously. Yet, in daily situations, goods available for choice are often presented or examined in sequence. Here we recorded neuronal activity in the primate orbitofrontal cortex alternating trials under simultaneous and under sequential offers. Our analyses demonstrate that the same neural circuit supports choices in the two modalities. Hence, current notions on the neuronal mechanisms underlying economic decisions generalize to choices under sequential offers.

Neuronal activity in dorsal anterior cingulate cortex during economic choices under variable action costs.

The role of the dorsal anterior cingulate cortex (ACCd) in decision making has often been discussed but remains somewhat unclear. On the one hand, numerous studies implicated this area in decisions driven by effort or action cost. On the other hand, work on economic choices between goods (under fixed action costs) found that neurons in ACCd encoded only post-decision variables. To advance our understanding of the role played by this area in decision making, we trained monkeys to choose between different goods (juice types) offered in variable amounts and with different action costs. Importantly, the task design dissociated computation of the action cost from planning of any particular action. Neurons in ACCd encoded the chosen value and the binary choice outcome in several reference frames (chosen juice, chosen cost, chosen action). Thus, this area provided a rich representation of post-decision variables. In contrast to the OFC, neurons in ACCd did not represent pre-decision variables such as individual offer values in any reference frame. Hence, ongoing decisions are unlikely guided by ACCd. Conversely, neuronal activity in this area might inform subsequent actions.

Values encoded in orbitofrontal cortex are causally related to economic choices.

In the eighteenth century, Daniel Bernoulli, Adam Smith and Jeremy Bentham proposed that economic choices rely on the computation and comparison of subjective values1. This hypothesis continues to inform modern economic theory2 and research in behavioural economics3, but behavioural measures are ultimately not sufficient to verify the proposal4. Consistent with the hypothesis, when agents make choices, neurons in the orbitofrontal cortex (OFC) encode the subjective value of offered and chosen goods5. Value-encoding cells integrate multiple dimensions6-9, variability in the activity of each cell group correlates with variability in choices10,11 and the population dynamics suggests the formation of a decision12. However, it is unclear whether these neural processes are causally related to choices. More generally, the evidence linking economic choices to value signals in the brain13-15 remains correlational16. Here we show that neuronal activity in the OFC is causal to economic choices. We conducted two experiments using electrical stimulation in rhesus monkeys (Macaca mulatta). Low-current stimulation increased the subjective value of individual offers and thus predictably biased choices. Conversely, high-current stimulation disrupted both the computation and the comparison of subjective values, and thus increased choice variability. These results demonstrate a causal chain linking subjective values encoded in OFC to valuation and choice.

Neural mechanisms of economic choices in mice.

Economic choices entail computing and comparing subjective values. Evidence from primates indicates that this behavior relies on the orbitofrontal cortex. Conversely, previous work in rodents provided conflicting results. Here we present a mouse model of economic choice behavior, and we show that the lateral orbital (LO) area is intimately related to the decision process. In the experiments, mice chose between different juices offered in variable amounts. Choice patterns closely resembled those measured in primates. Optogenetic inactivation of LO dramatically disrupted choices by inducing erratic changes of relative value and by increasing choice variability. Neuronal recordings revealed that different groups of cells encoded the values of individual options, the binary choice outcome and the chosen value. These groups match those previously identified in primates, except that the neuronal representation in mice is spatial (in monkeys it is good-based). Our results lay the foundations for a circuit-level analysis of economic decisions.

Neuronal Activity in the Primate Amygdala during Economic Choice.

Multiple lines of evidence link economic choices to the orbitofrontal cortex (OFC), but other brain regions may contribute to the computation and comparison of economic values. A particularly strong candidate is the basolateral amygdala (BLA). Amygdala lesions impair performance in reinforcer devaluation tasks, suggesting that the BLA contributes to value computation. Furthermore, previous studies of the BLA have found neuronal activity consistent with a value representation. Here, we recorded from the BLA of two male rhesus macaques choosing between different juices. Offered quantities varied from trial to trial, and relative values were inferred from choices. Approximately one-third of BLA cells were task-related. Our analyses revealed the presence of three groups of neurons encoding variables offer value, chosen value, and chosen juice In this respect, the BLA appeared similar to the OFC. The two areas differed for the proportion of neurons in each group, as the fraction of chosen value cells was significantly higher in the BLA. Importantly, the activity of these neurons reflected the subjective nature of value. Firing rates in the BLA were sustained throughout the trial and maximal after juice delivery. In contrast, firing rates in the OFC were phasic and maximal shortly after offer presentation. Our results suggest that the BLA supports economic choice and reward expectation.SIGNIFICANCE STATEMENT Economic choices rely on the orbitofrontal cortex (OFC), but other brain regions may contribute to this behavior. A strong candidate is the basolateral amygdala (BLA). Previous results are consistent with a neuronal representation of value, but the role of the BLA in economic decisions remains unclear. Here, we recorded from monkeys choosing between juices. Neurons in the BLA encoded three decision variables: offer value, chosen value, and chosen juice These variables were also identified in the OFC. The two areas differed in the proportion of cells encoding each variable and in the activation timing. In the OFC, firing rates peaked shortly after offer presentation; in the BLA, firing rates were sustained and peaked after juice delivery. These results suggest that the BLA supports choices and reward expectation.

Economic Decisions through Circuit Inhibition.

Economic choices between goods are thought to rely on the orbitofrontal cortex (OFC), but the decision mechanisms remain poorly understood. To shed light on this fundamental issue, we recorded from the OFC of monkeys choosing between two juices offered sequentially. An analysis of firing rates across time windows revealed the presence of different groups of neurons similar to those previously identified under simultaneous offers. This observation suggested that economic decisions in the two modalities are formed in the same neural circuit. We then examined several hypotheses on the decision mechanisms. OFC neurons encoded good identities and values in a juice-based representation (labeled lines). Contrary to previous assessments, our data argued against the idea that decisions rely on mutual inhibition at the level of offer values. In fact, we showed that previous arguments for mutual inhibition were confounded by differences in value ranges. Instead, decisions seemed to involve mechanisms of circuit inhibition, whereby each offer value indirectly inhibited neurons encoding the opposite choice outcome. Our results reconcile a variety of previous findings and provide a general account for the neuronal underpinnings of economic choices.

Categorical encoding of decision variables in orbitofrontal cortex.

A fundamental and recurrent question in systems neuroscience is that of assessing what variables are encoded by a given population of neurons. Such assessments are often challenging because neurons in one brain area may encode multiple variables, and because neuronal representations might be categorical or non-categorical. These issues are particularly pertinent to the representation of decision variables in the orbitofrontal cortex (OFC)-an area implicated in economic choices. Here we present a new algorithm to assess whether a neuronal representation is categorical or non-categorical, and to identify the encoded variables if the representation is indeed categorical. The algorithm is based on two clustering procedures, one variable-independent and the other variable-based. The two partitions are then compared through adjusted mutual information. The present algorithm overcomes limitations of previous approaches and is widely applicable. We tested the algorithm on synthetic data and then used it to examine neuronal data recorded in the primate OFC during economic decisions. Confirming previous assessments, we found the neuronal representation in OFC to be categorical in nature. We also found that neurons in this area encode the value of individual offers, the binary choice outcome and the chosen value. In other words, during economic choice, neurons in the primate OFC encode decision variables in a categorical way.

Partial Adaptation to the Value Range in the Macaque Orbitofrontal Cortex.

Values available for choice in different behavioral contexts can vary immensely. To compensate for this variability, neuronal circuits underlying economic decisions undergo adaptation. In orbitofrontal cortex (OFC), neurons encode the subjective value of offered and chosen goods in a quasilinear way. Previous experiments found that the gain of the encoding is lower when the value range is wider. However, the parameters OFC neurons adapted to remained unclear. Furthermore, previous studies did not examine additive changes in neuronal responses. Computational considerations indicate that these factors can directly impact choice behavior. Here we investigated how OFC neurons adapt to changes in the value range. We recorded from two male rhesus monkeys during a juice choice task. Each session was divided into two blocks of trials. In each block, juices were offered within a set range of values, and ranges changed between blocks. Across blocks, neuronal responses adapted to both the maximum and the minimum value, but only partially. As a result, the minimum neural activity was elevated in some value ranges relative to others. Through simulation of a linear decision model, we showed that increasing the minimum response increases choice variability, lowering the expected payoff. This effect is modulated by the balance between cells with positive and negative encoding. The presence of these two populations induces a non-monotonic relationship between the value range and choice efficacy, such that the expected payoff is highest for decisions in an intermediate value range.SIGNIFICANCE STATEMENT Economic decisions are thought to rely on the orbitofrontal cortex (OFC). The values available for choice vary enormously in different contexts. Previous work showed that neurons in OFC encode values in a linear way, and that the gain of encoding is inversely related to the range of available values. However, the specific parameters driving adaptation remained unclear. Here we show that OFC neurons adapt to both the maximum and minimum value in the current context. However, adaptation is partial, leading to contextual changes in the response offset. Interestingly, increasing the activity offset negatively affects choices in a simulated network. Partial adaptation may allow the circuit to maintain information about context value at the cost of slightly reduced payoff.

Neuronal evidence for good-based economic decisions under variable action costs.

Previous work showed that economic decisions can be made independently of spatial contingencies. However, when goods available for choice bear different action costs, the decision necessarily reflects aspects of the action. One possibility is that "stimulus values" are combined with the corresponding action costs in a motor representation, and decisions are then made in actions space. Alternatively, action costs could be integrated with other determinants of value in a non-spatial representation. If so, decisions under variable action costs could take place in goods space. Here, we recorded from orbitofrontal cortex while monkeys chose between different juices offered in variable amounts. We manipulated action costs by varying the saccade amplitude, and we dissociated in time and space offer presentation from action planning. Neurons encoding the binary choice outcome did so well before the presentation of saccade targets, indicating that decisions were made in goods space.

Orbitofrontal Cortex: A Neural Circuit for Economic Decisions.

Economic choice behavior entails the computation and comparison of subjective values. A central contribution of neuroeconomics has been to show that subjective values are represented explicitly at the neuronal level. With this result at hand, the field has increasingly focused on the difficult question of where in the brain and how exactly subjective values are compared to make a decision. Here, we review a broad range of experimental and theoretical results suggesting that good-based decisions are generated in a neural circuit within the orbitofrontal cortex (OFC). The main lines of evidence supporting this proposal include the fact that goal-directed behavior is specifically disrupted by OFC lesions, the fact that different groups of neurons in this area encode the input and the output of the decision process, the fact that activity fluctuations in each of these cell groups correlate with choice variability, and the fact that these groups of neurons are computationally sufficient to generate decisions. Results from other brain regions are consistent with the idea that good-based decisions take place in OFC and indicate that value signals inform a variety of mental functions. We also contrast the present proposal with other leading models for the neural mechanisms of economic decisions. Finally, we indicate open questions and suggest possible directions for future research.

Optimal coding and neuronal adaptation in economic decisions.

During economic decisions, offer value cells in orbitofrontal cortex (OFC) encode the values of offered goods. Furthermore, their tuning functions adapt to the range of values available in any given context. A fundamental and open question is whether range adaptation is behaviorally advantageous. Here we present a theory of optimal coding for economic decisions. We propose that the representation of offer values is optimal if it ensures maximal expected payoff. In this framework, we examine offer value cells in non-human primates. We show that their responses are quasi-linear even when optimal tuning functions are highly non-linear. Most importantly, we demonstrate that for linear tuning functions range adaptation maximizes the expected payoff. Thus value coding in OFC is functionally rigid (linear tuning) but parametrically plastic (range adaptation with optimal gain). Importantly, the benefit of range adaptation outweighs the cost of functional rigidity. While generally suboptimal, linear tuning may facilitate transitive choices.

Neuronal remapping and circuit persistence in economic decisions.

The orbitofrontal cortex plays a central role in good-based economic decisions. When subjects make choices, neurons in this region represent the identities and values of offered and chosen goods. Notably, choices in different behavioral contexts may involve a potentially infinite variety of goods. Thus a fundamental question concerns the stability versus flexibility of the decision circuit. Here we show in rhesus monkeys that neurons encoding the identity or the subjective value of particular goods in a given context 'remap' and become associated with different goods when the context changes. At the same time, the overall organization of the decision circuit and the function of individual cells remain stable across contexts. In particular, two neurons supporting the same decision in one context also support the same decision in different contexts. These results demonstrate how the same neural circuit can underlie economic decisions involving a large variety of goods.

Dialogue on economic choice, learning theory, and neuronal representations.

In recent years, two distinct lines of work have focused on the substrates of associative learning and on the mechanisms of economic decisions. While experiments often focused the same brain regions - most notably the orbitofrontal cortex - the two literatures have remained largely distinct. Here we engage in a dialogue with the intent to clarify the relationship between the two frameworks. We identify a potential correspondence between the concept of outcome defined in learning theory and that of good defined in neuroeconomics, and we specifically discuss the concept of value defined in the two frameworks. While many differences remain unresolved, a common idea is that good/outcome values are subjective, devaluation-sensitive and computed on the fly, not "cached" or pre-computed.