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.

Parallel Pathways Provide Hippocampal Spatial Information to Prefrontal Cortex.

Long-range synaptic connections define how information flows through neuronal networks. Here, we combined retrograde and anterograde trans-synaptic viruses to delineate areas that exert direct and indirect influence over the dorsal and ventral prefrontal cortex (PFC) of the rat (both sexes). Notably, retrograde tracing using pseudorabies virus (PRV) revealed that both dorsal and ventral areas of the PFC receive prominent disynaptic input from the dorsal CA3 (dCA3) region of the hippocampus. The PRV experiments also identified candidate anatomical relays for this disynaptic pathway, namely, the ventral hippocampus, lateral septum, thalamus, amygdala, and basal forebrain. To determine the viability of each of these relays, we performed three additional experiments. In the first, we injected the retrograde monosynaptic tracer Fluoro-Gold into the PFC and the anterograde monosynaptic tracer Fluoro-Ruby into the dCA3 to confirm the first-order connecting areas and revealed several potential relay regions between the PFC and dCA3. In the second, we combined PRV injection in the PFC with polysynaptic anterograde viral tracer (HSV-1) in the dCA3 to reveal colabeled connecting neurons, which were evident only in the ventral hippocampus. In the third, we combined retrograde adeno-associated virus (AAV) injections in the PFC with an anterograde AAV in the dCA3 to reveal anatomical relay neurons in the ventral hippocampus and dorsal lateral septum. Together, these findings reveal parallel disynaptic pathways from the dCA3 to the PFC, illuminating a new anatomical framework for understanding hippocampal-prefrontal interactions. We suggest that the representation of context and space may be a universal feature of prefrontal function.SIGNIFICANCE STATEMENT The known functions of the prefrontal cortex are shaped by input from multiple brain areas. We used transneuronal viral tracing to discover multiple prominent disynaptic pathways through which the dorsal hippocampus (specifically, the dorsal CA3) has the potential to shape the actions of the prefrontal cortex. The demonstration of neuronal relays in the ventral hippocampus and lateral septum presents a new foundation for understanding long-range influences over prefrontal interactions, including the specific contribution of the dorsal CA3 to prefrontal function.

Heterogeneous value coding in orbitofrontal populations.

Value signals in the brain are important for learning, decision-making, and orienting behavior toward relevant goals. Although they can play different roles in behavior and cognition, value representations are often considered to be uniform and static signals. Nonetheless, contextual and mixed representations of value have been widely reported. Here, we review the evidence for heterogeneity in value coding and dynamics in the orbitofrontal cortex. We argue that this diversity plays a key role in the representation of value itself and allows neurons to integrate value with other behaviorally relevant information. We also discuss modeling approaches that can dissociate potential functions of heterogeneous value codes and provide further insight into its importance in behavior and cognition. (PsycInfo Database Record (c) 2021 APA, all rights reserved).

Identifying identity and attributing value to attributes: reconsidering mechanisms of preference decisions.

Although the orbitofrontal cortex (OFC) robustly encodes value during preference decisions, it also encodes multiple non-value features of choice options. The role of this information, and its relationship to the options' overall value remain open questions. In this opinion, we attempt to disentangle oft-studied categories of option information - identity and attributes - in the context of both classic theories of economic choice and contradicting evidence of choice biases in multi-attribute decisions. In doing so, we aim to set forth considerations for understanding the wide variety of decision-relevant information encoded by the OFC during preference decisions.