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.

Making Sense of the Multiplicity and Dynamics of Navigational Codes in the Brain.

Since the discovery of conspicuously spatially tuned neurons in the hippocampal formation over 50 years ago, characterizing which, where, and how neurons encode navigationally relevant variables has been a major thrust of navigational neuroscience. While much of this effort has centered on the hippocampal formation and functionally-adjacent structures, recent work suggests that spatial codes, in some form or another, can be found throughout the brain, even in areas traditionally associated with sensation, movement, and executive function. In this review, we highlight these unexpected results, draw insights from comparison of these codes across contexts, regions, and species, and finally suggest an avenue for future work to make sense of these diverse and dynamic navigational codes.

Optogenetic suppression of the nucleus reuniens selectively impairs encoding during spatial working memory.

The nucleus reuniens (Re) of the ventral midline thalamus is known to be a critical anatomical link between the hippocampus (HPC) and the medial prefrontal cortex (mPFC). Consistent with this anatomical connectivity, the Re has been shown to be crucial for HPC-mPFC oscillatory synchrony. Moreover, Re inhibition consistently results in spatial working memory (SWM) deficits. Together, these results suggest that SWM requires HPC-mPFC synchrony via the Re. In spite of these findings, an understanding of how the Re contributes to the encoding, maintenance, and retrieval of spatial information during a SWM task is lacking. To address this issue, we trained rats to perform a SWM-dependent delayed-non-match-to-position (DNMP) task in a T-maze. Using optogenetic inhibition of Re activity, we demonstrated that Re suppression during the sample phase, but not the delay or choice phase, significantly decreased choice accuracy. We conclude that the Re contributes to the encoding of spatial information during working memory.

Neural timescales reflect behavioral demands in freely moving rhesus macaques.

Previous work demonstrated a highly reproducible cortical hierarchy of neural timescales at rest, with sensory areas displaying fast, and higher-order association areas displaying slower timescales. The question arises how such stable hierarchies give rise to adaptive behavior that requires flexible adjustment of temporal coding and integration demands. Potentially, this lack of variability in the hierarchical organization of neural timescales could reflect the structure of the laboratory contexts. We posit that unconstrained paradigms are ideal to test whether the dynamics of neural timescales reflect behavioral demands. Here we measured timescales of local field potential activity while male rhesus macaques foraged in an open space. We found a hierarchy of neural timescales that differs from previous work. Importantly, although the magnitude of neural timescales expanded with task engagement, the brain areas' relative position in the hierarchy was stable. Next, we demonstrated that the change in neural timescales is dynamic and contains functionally-relevant information, differentiating between similar events in terms of motor demands and associated reward. Finally, we demonstrated that brain areas are differentially affected by these behavioral demands. These results demonstrate that while the space of neural timescales is anatomically constrained, the observed hierarchical organization and magnitude is dependent on behavioral demands.

Hierarchical action encoding in prefrontal cortex of freely moving macaques.

Our natural behavioral repertoires include coordinated actions of characteristic types. To better understand how neural activity relates to the expression of actions and action switches, we studied macaques performing a freely moving foraging task in an open environment. We developed a novel analysis pipeline that can identify meaningful units of behavior, corresponding to recognizable actions such as sitting, walking, jumping, and climbing. On the basis of transition probabilities between these actions, we found that behavior is organized in a modular and hierarchical fashion. We found that, after regressing out many potential confounders, actions are associated with specific patterns of firing in each of six prefrontal brain regions and that, overall, encoding of action category is progressively stronger in more dorsal and more caudal prefrontal regions. Together, these results establish a link between selection of units of primate behavior on one hand and neuronal activity in prefrontal regions on the other.

Hierarchical organization of rhesus macaque behavior.

Primatologists, psychologists and neuroscientists have long hypothesized that primate behavior is highly structured. However, delineating that structure has been impossible due to the difficulties of precision behavioral tracking. Here we analyzed a dataset consisting of continuous measures of the 3D position of two male rhesus macaques (Macaca mulatta) performing three different tasks in a large unrestrained environment over several hours. Using an unsupervised embedding approach on the tracked joints, we identified commonly repeated pose patterns, which we call postures. We found that macaques' behavior is characterized by 49 distinct postures, lasting an average of 0.6 seconds. We found evidence that behavior is hierarchically organized, in that transitions between poses tend to occur within larger modules, which correspond to identifiable actions; these actions are further organized hierarchically. Our behavioral decomposition allows us to identify universal (cross-individual and cross-task) and unique (specific to each individual and task) principles of behavior. These results demonstrate the hierarchical nature of primate behavior, provide a method for the automated ethogramming of primate behavior, and provide important constraints on neural models of pose generation.

Widespread coding of navigational variables in prefrontal cortex.

To navigate effectively, we must represent information about our location in the environment. Traditional research highlights the role of the hippocampal complex in this process. Spurred by recent research highlighting the widespread cortical encoding of cognitive and motor variables previously thought to have localized function, we hypothesized that navigational variables would be likewise encoded widely, especially in the prefrontal cortex, which is associated with volitional behavior. We recorded neural activity from six prefrontal regions while macaques performed a foraging task in an open enclosure. In all regions, we found strong encoding of allocentric position, allocentric head direction, boundary distance, and linear and angular velocity. These encodings were not accounted for by distance, time to reward, or motor factors. The strength of coding of all variables increased along a ventral-to-dorsal gradient. Together, these results argue that encoding of navigational variables is not localized to the hippocampus and support the hypothesis that navigation is continuous with other forms of flexible cognition in the service of action.

Choice-relevant information transformation along a ventrodorsal axis in the medial prefrontal cortex.

Choice-relevant brain regions in prefrontal cortex may progressively transform information about options into choices. Here, we examine responses of neurons in four regions of the medial prefrontal cortex as macaques performed two-option risky choices. All four regions encode economic variables in similar proportions and show similar putative signatures of key choice-related computations. We provide evidence to support a gradient of function that proceeds from areas 14 to 25 to 32 to 24. Specifically, we show that decodability of twelve distinct task variables increases along that path, consistent with the idea that regions that are higher in the anatomical hierarchy make choice-relevant variables more separable. We also show progressively longer intrinsic timescales in the same series. Together these results highlight the importance of the medial wall in choice, endorse a specific gradient-based organization, and argue against a modular functional neuroanatomy of choice.