Multiattribute Decision-making in Macaques Relies on Direct Attribute Comparisons.

In value-based decisions, there are frequently multiple attributes, such as cost, quality, or quantity, that contribute to the overall goodness of an option. Because one option may not be better in all attributes at once, the decision process should include a means of weighing relevant attributes. Most decision-making models solve this problem by computing an integrated value, or utility, for each option from a weighted combination of attributes. However, behavioral anomalies in decision-making, such as context effects, indicate that other attribute-specific computations might be taking place. Here, we tested whether rhesus macaques show evidence of attribute-specific processing in a value-based decision-making task. Monkeys made a series of decisions involving choice options comprising a sweetness and probability attribute. Each attribute was represented by a separate bar with one of two mappings between bar size and the magnitude of the attribute (i.e., bigger = better or bigger = worse). We found that translating across different mappings produced selective impairments in decision-making. Choices were less accurate and preferences were more variable when like attributes differed in mapping, suggesting that preventing monkeys from easily making direct attribute comparisons resulted in less accurate choice behavior. This was not the case when mappings of unalike attributes within the same option were different. Likewise, gaze patterns favored transitions between like attributes over transitions between unalike attributes of the same option, so that like attributes were sampled sequentially to support within-attribute comparisons. Together, these data demonstrate that value-based decisions rely, at least in part, on directly comparing like attributes of multiattribute options.

Multi-attribute decision-making in macaques relies on direct attribute comparisons.

In value-based decisions, there are frequently multiple attributes, such as cost, quality, or quantity, that contribute to the overall goodness of an option. Since one option may not be better in all attributes at once, the decision process should include a means of weighing relevant attributes. Most decision-making models solve this problem by computing an integrated value, or utility, for each option from a weighted combination of attributes. However, behavioral anomalies in decision-making, such as context effects, indicate that other attribute-specific computations might be taking place. Here, we tested whether rhesus macaques show evidence of attribute-specific processing in a value-based decision-making task. Monkeys made a series of decisions involving choice options comprising a sweetness and probability attribute. Each attribute was represented by a separate bar with one of two mappings between bar size and the magnitude of the attribute (i.e., bigger=better or bigger=worse). We found that translating across different mappings produced selective impairments in decision-making. When like attributes differed, monkeys were prevented from easily making direct attribute comparisons, and choices were less accurate and preferences were more variable. This was not the case when mappings of unalike attributes within the same option were different. Likewise, gaze patterns favored transitions between like attributes over transitions between unalike attributes of the same option, so that like attributes were sampled sequentially to support within-attribute comparisons. Together, these data demonstrate that value-based decisions rely, at least in part, on directly comparing like attributes of multi-attribute options. Significance Statement: Value-based decision-making is a cognitive function impacted by a number of clinical conditions, including substance use disorder and mood disorders. Understanding the neural mechanisms, including online processing steps involved in decision formation, will provide critical insights into decision-making deficits characteristic of human psychiatric disorders. Using rhesus monkeys as a model species capable of complex decision-making, this study shows that decisions involve a process of comparing like features, or attributes, of multi-attribute options. This is contrary to popular models of decision-making in which attributes are first combined into an overall value, or utility, to make a choice. Therefore, these results serve as an important foundation for establishing a more complete understanding of the neural mechanisms involved in forming complex decisions.

Excitatory and Inhibitory Signaling in the Nucleus Accumbens Encode Different Aspects of a Pavlovian Cue in Sign Tracking and Goal Tracking Rats.

When a Pavlovian cue is presented separately from its associated reward, some animals will acquire a sign tracking (ST) response - approach and/or interaction with the cue - while others will acquire a goal tracking response - approach to the site of reward. We have previously shown that cue-evoked excitations in the nucleus accumbens (NAc) encode the vigor of both behaviors; in contrast, reward-related responses diverge over the course of training, possibly reflecting neurochemical differences between sign tracker and goal tracker individuals. However, a substantial subset of neurons in the NAc exhibit inhibitory, rather than excitatory, cue-evoked responses, and the evolution of their signaling during Pavlovian conditioning remains unknown. Using single-neuron recordings in behaving rats, we show that NAc neurons with cue-evoked inhibitions have distinct coding properties from neurons with cue-evoked excitations. Cue-evoked inhibitions become more numerous over the course of training and, like excitations, may encode the vigor of sign tracking and goal tracking behavior. However, the responses of cue-inhibited neurons do not evolve differently between sign tracker and goal tracker individuals. Moreover, cue-evoked inhibitions, unlike excitations, are insensitive to extinction of the cue-reward relationship. Finally, we show that cue-evoked excitations are greatly diminished by reward devaluation, while inhibitory cue responses are virtually unaffected. Overall, these findings converge with existing evidence that cue-excited neurons in NAc, but not cue-inhibited neurons, are profoundly sensitive to the same behavior variations that are often associated with changes in dopamine release.

Sign Tracking and Goal Tracking Are Characterized by Distinct Patterns of Nucleus Accumbens Activity.

During Pavlovian conditioning, if a cue (e.g., lever extension) predicts reward delivery in a different location (e.g., a food magazine), some individuals will come to approach and interact with the cue, a behavior known as sign tracking (ST), and others will approach the site of reward, a behavior known as goal tracking (GT). In rats, the acquisition of ST versus GT behavior is associated with distinct profiles of dopamine release in the nucleus accumbens (NAc), but it is unknown whether it is associated with different patterns of accumbens neural activity. Therefore, we recorded from individual neurons in the NAc core during the acquisition, maintenance, and extinction of ST and GT behavior. Even though NAc dopamine is specifically important for the acquisition and expression of ST, we found that cue-evoked excitatory responses encode the vigor of both ST and GT behavior. In contrast, among sign trackers only, there was a prominent decrease in reward-related activity over the course of training, which may reflect the decreasing reward prediction error encoded by phasic dopamine. Finally, both behavior and cue-evoked activity were relatively resistant to extinction in sign trackers, as compared with goal trackers, although a subset of neurons in both groups retained their cue-evoked responses. Overall, the results point to the convergence of multiple forms of reward learning in the NAc.