Brain mechanism of foraging: Reward-dependent synaptic plasticity versus neural integration of values.

During foraging behavior, action values are persistently encoded in neural activity and updated depending on the history of choice outcomes. What is the neural mechanism for action value maintenance and updating? Here, we explore two contrasting network models: synaptic learning of action value versus neural integration. We show that both models can reproduce extant experimental data, but they yield distinct predictions about the underlying biological neural circuits. In particular, the neural integrator model but not the synaptic model requires that reward signals are mediated by neural pools selective for action alternatives and their projections are aligned with linear attractor axes in the valuation system. We demonstrate experimentally observable neural dynamical signatures and feasible perturbations to differentiate the two contrasting scenarios, suggesting that the synaptic model is a more robust candidate mechanism. Overall, this work provides a modeling framework to guide future experimental research on probabilistic foraging.

Bifurcation in space: Emergence of function modularity in the neocortex.

How does functional modularity emerge in a multiregional cortex made with repeats of a canonical local circuit architecture? We investigated this question by focusing on neural coding of working memory, a core cognitive function. Here we report a mechanism dubbed "bifurcation in space", and show that its salient signature is spatially localized "critical slowing down" leading to an inverted V-shaped profile of neuronal time constants along the cortical hierarchy during working memory. The phenomenon is confirmed in connectome-based large-scale models of mouse and monkey cortices, offering an experimentally testable prediction to assess whether working memory representation is modular. Many bifurcations in space could explain the emergence of different activity patterns potentially deployed for distinct cognitive functions, This work demonstrates that a distributed mental representation is compatible with functional specificity as a consequence of macroscopic gradients of neurobiological properties across the cortex, suggesting a general principle for understanding brain's modular organization.

Metastable attractors explain the variable timing of stable behavioral action sequences.

The timing of self-initiated actions shows large variability even when they are executed in stable, well-learned sequences. Could this mix of reliability and stochasticity arise within the same neural circuit? We trained rats to perform a stereotyped sequence of self-initiated actions and recorded neural ensemble activity in secondary motor cortex (M2), which is known to reflect trial-by-trial action-timing fluctuations. Using hidden Markov models, we established a dictionary between activity patterns and actions. We then showed that metastable attractors, representing activity patterns with a reliable sequential structure and large transition timing variability, could be produced by reciprocally coupling a high-dimensional recurrent network and a low-dimensional feedforward one. Transitions between attractors relied on correlated variability in this mesoscale feedback loop, predicting a specific structure of low-dimensional correlations that were empirically verified in M2 recordings. Our results suggest a novel mesoscale network motif based on correlated variability supporting naturalistic animal behavior.

From synapse to network: models of information storage and retrieval in neural circuits.

The mechanisms of information storage and retrieval in brain circuits are still the subject of debate. It is widely believed that information is stored at least in part through changes in synaptic connectivity in networks that encode this information and that these changes lead in turn to modifications of network dynamics, such that the stored information can be retrieved at a later time. Here, we review recent progress in deriving synaptic plasticity rules from experimental data and in understanding how plasticity rules affect the dynamics of recurrent networks. We show that the dynamics generated by such networks exhibit a large degree of diversity, depending on parameters, similar to experimental observations in vivo during delayed response tasks.