Abstract Value Encoding in Neural Populations But Not Single Neurons.

An important open question in neuroeconomics is how the brain represents the value of offers in a way that is both abstract (allowing for comparison) and concrete (preserving the details of the factors that influence value). Here, we examine neuronal responses to risky and safe options in five brain regions that putatively encode value in male macaques. Surprisingly, we find no detectable overlap in the neural codes used for risky and safe options, even when the options have identical subjective values (as revealed by preference) in any of the regions. Indeed, responses are weakly correlated and occupy distinct (semi-orthogonal) encoding subspaces. Notably, however, these subspaces are linked through a linear transform of their constituent encodings, a property that allows for comparison of dissimilar option types. This encoding scheme allows these regions to multiplex decision related processes: they can encode the detailed factors that influence offer value (here, risky and safety) but also directly compare dissimilar offer types. Together these results suggest a neuronal basis for the qualitatively different psychological properties of risky and safe options and highlight the power of population geometry to resolve outstanding problems in neural coding.SIGNIFICANCE STATEMENT To make economic choices, we must have some mechanism for comparing dissimilar offers. We propose that the brain uses distinct neural codes for risky and safe offers, but that these codes are linearly transformable. This encoding scheme has the dual advantage of allowing for comparison across offer types while preserving information about offer type, which in turn allows for flexibility in changing circumstances. We show that responses to risky and safe offers exhibit these predicted properties in five different reward-sensitive regions. Together, these results highlight the power of population coding principles for solving representation problems in economic choice.

A structural and functional subdivision in central orbitofrontal cortex.

Economic choice requires many cognitive subprocesses, including stimulus detection, valuation, motor output, and outcome monitoring; many of these subprocesses are associated with the central orbitofrontal cortex (cOFC). Prior work has largely assumed that the cOFC is a single region with a single function. Here, we challenge that unified view with convergent anatomical and physiological results from rhesus macaques. Anatomically, we show that the cOFC can be subdivided according to its much stronger (medial) or weaker (lateral) bidirectional anatomical connectivity with the posterior cingulate cortex (PCC). We call these subregions cOFCm and cOFCl, respectively. These two subregions have notable functional differences. Specifically, cOFCm shows enhanced functional connectivity with PCC, as indicated by both spike-field coherence and mutual information. The cOFCm-PCC circuit, but not the cOFCl-PCC circuit, shows signatures of relaying choice signals from a non-spatial comparison framework to a spatially framed organization and shows a putative bidirectional mutually excitatory pattern.

Latent learning, cognitive maps, and curiosity.

Curiosity is a desire for information that is not motivated by strategic concerns. Latent learning is not driven by standard reinforcement processes. We propose that curiosity serves the purpose of motivating latent learning. While latent learning is often treated as a passive or incidental process, it normally reflects a strong evolved pressure to actively seek large amounts of information. That information in turn allows curious decision makers to represent the structure of their environment, that is, to form cognitive maps. These cognitive maps then drive adaptive flexible behavior. Based on recent data, we propose that orbitofrontal cortex (OFC) and dorsal anterior cingulate cortex (dACC) play complementary roles in curiosity-driven learning. Specifically, we propose that (1) OFC tracks intrinsic value of information and incorporates new information into a cognitive map; and (2) dACC tracks the environmental demands and information availability to then use the cognitive map from OFC to guide behavior.

Using rAAV2-retro in rhesus macaques: Promise and caveats for circuit manipulation.

BACKGROUND: Recent genetic technologies such as opto- and chemogenetics allow for the manipulation of brain circuits with unprecedented precision. Most studies employing these techniques have been undertaken in rodents, but a more human-homologous model for studying the brain is the nonhuman primate (NHP). Optimizing viral delivery of transgenes encoding actuator proteins could revolutionize the way we study neuronal circuits in NHPs. NEW METHOD: rAAV2-retro, a popular new capsid variant, produces robust retrograde labeling in rodents. Whether rAAV2-retro's highly efficient retrograde transport would translate to NHPs was unknown. Here, we characterized the anatomical distribution of labeling following injections of rAAV2-retro encoding opsins or DREADDs in the cortico-basal ganglia and oculomotor circuits of rhesus macaques. RESULTS: rAAV2-retro injections in striatum, frontal eye field, and superior colliculus produced local labeling at injection sites and robust retrograde labeling in many afferent regions. In every case, however, a few brain regions with well-established projections to the injected structure lacked retrogradely labeled cells. We also observed robust terminal field labeling in downstream structures. COMPARISON WITH EXISTING METHOD(S): Patterns of labeling were similar to those obtained with traditional tract-tracers, except for some afferent labeling that was noticeably absent. CONCLUSIONS: rAAV2-retro promises to be useful for circuit manipulation via retrograde transduction in NHPs, but caveats were revealed by our findings. Some afferently connected regions lacked retrogradely labeled cells, showed robust axon terminal labeling, or both. This highlights the importance of anatomically characterizing rAAV2-retro's expression in target circuits in NHPs before moving to manipulation studies.

Beyond "incentive hope": Information sampling and learning under reward uncertainty.

Information seeking, especially when motivated by strategic learning and intrinsic curiosity, could render the new mechanism "incentive hope" proposed by Anselme & Güntürkün sufficient, but not necessary to explain how reward uncertainty promotes reward seeking and consumption. Naturalistic and foraging-like tasks can help parse motivational processes that bridge learning and foraging behaviors and identify their neural underpinnings.

Monkeys are curious about counterfactual outcomes.

Many non-human animals show exploratory behaviors. It remains unclear whether any possess human-like curiosity. We previously proposed three criteria for applying the term curiosity to animal behavior: (1) the subject is willing to sacrifice reward to obtain information, (2) the information provides no immediate instrumental or strategic benefit, and (3) the amount the subject is willing to pay depends systematically on the amount of information available. In previous work on information-seeking in animals, information generally predicts upcoming rewards, and animals' decisions may therefore be a byproduct of reinforcement processes. Here we get around this potential confound by taking advantage of macaques' ability to reason counterfactually (that is, about outcomes that could have occurred had the subject chosen differently). Specifically, macaques sacrificed fluid reward to obtain information about counterfactual outcomes. Moreover, their willingness to pay scaled with the information (Shannon entropy) offered by the counterfactual option. These results demonstrate the existence of human-like curiosity in non-human primates according to our criteria, which circumvent several confounds associated with less stringent criteria.

Reactivation of associative structure specific outcome responses during prospective evaluation in reward-based choices.

Before making a reward-based choice, we must evaluate each option. Some theories propose that prospective evaluation involves a reactivation of the neural response to the outcome. Others propose that it calls upon a response pattern that is specific to each underlying associative structure. We hypothesize that these views are reconcilable: during prospective evaluation, offers reactivate neural responses to outcomes that are unique to each associative structure; when the outcome occurs, this pattern is activated, simultaneously, with a general response to the reward. We recorded single-units from macaque orbitofrontal cortex (Area 13) in a riskless choice task with interleaved described and experienced offer trials. Here we report that neural activations to offers and their outcomes overlap, as do neural activations to the outcomes on the two trial types. Neural activations to experienced and described offers are unrelated even though they predict the same outcomes. Our reactivation theory parsimoniously explains these results.

Differential effects of social and novelty enrichment on individual differences in impulsivity and behavioral flexibility.

Early life experience profoundly impacts behavior and cognitive functions in rats. The present study investigated how the presence of conspecifics and/or novel objects, could independently influence individual differences in impulsivity and behavioral flexibility. Twenty-four rats were reared in an isolated condition, an isolated condition with a novel object, a pair-housed social condition, or a pair-housed social condition with a novel object. The rats were then tested on an impulsive choice task, a behavioral flexibility task, and an impulsive action task. Novelty enrichment produced an overall increase in impulsive choice, while social enrichment decreased impulsive choice in the absence of novelty enrichment and also produced an overall increase in impulsive action. In the behavioral flexibility task, social enrichment increased regressive errors, whereas both social and novelty enrichment reduced never-reinforced errors. Individual differences analyses indicated a significant relationship between performance in the behavioral flexibility and impulsive action tasks, which may reflect a common psychological correlate of action inhibition. Moreover, there was a relationship between delay sensitivity in the impulsive choice task and performance on the DRL and behavioral flexibility tasks, suggesting a dual role for timing and inhibitory processes in driving the interrelationship between these tasks. Overall, these results indicate that social and novelty enrichment produce distinct effects on impulsivity and adaptability, suggesting the need to parse out the different elements of enrichment in future studies. Further research is warranted to better understand how individual differences in sensitivity to enrichment affect individuals' interactions with and the resulting consequences of the rearing environment.