Multiple gates on working memory

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Highlights

  • Real-world scenarios require control over working memory input, output, and contents.

  • Frontostriatal circuits solve these issues via dynamics evolved for motor selection.

  • Output and reallocation of working memory may be critical for thought and planning.

The contexts for action may be only transiently visible, accessible, and relevant. The cortico-basal ganglia (BG) circuit addresses these demands by allowing the right motor plans to drive action at the right times, via a BG-mediated gate on motor representations. A long-standing hypothesis posits these same circuits are replicated in more rostral brain regions to support gating of cognitive representations. Key evidence now supports the prediction that BG can act as a gate on the input to working memory, as a gate on its output, and as a means of reallocating working memory representations rendered irrelevant by recent events. These discoveries validate key tenets of many computational models, circumscribe motor and cognitive models of recurrent cortical dynamics alone, and identify novel directions for research on the mechanisms of higher-level cognition.

Introduction

The world is rich with information, much of it only transiently available to the senses. And yet, an animal must leverage a small, but crucial, fraction of this input in order to provide a context for its behavior. Working memory is a central adaptation to confront this problem, selecting behaviorally relevant information, maintaining it in time, and referencing it when appropriate in order to make decisions about how to act in the world. Indeed, the elaborated working memory system of higher primates partly underlies their distinguishing intelligence and flexible behavior.

Working memory is capacity limited. Measures of capacity predict individual differences in cognitive ability, including scholastic aptitude, intelligence, and aging-related cognitive change 1, 2. Moreover, changes in working memory capacity accompany neurological and psychiatric disease [3] and may underlie behavioral and cognitive deficits associated with these disorders [4]. However, just as the world is dynamic, so is the working memory system adapted to address these dynamics. Thus, control processes are required in order to rapidly and selectively store information in memory (input control), to rapidly and selectively deploy subsets of that information for use in behavior (output control), and to selectively eliminate an obsolete representation from memory when its predicted utility declines (reallocation). Such control functions would seem to be crucial for strategically making use of capacity-limited working memory. And indeed, though less understood, individual differences in these control processes could be equally or even more important than the size of a static capacity for intellectual ability.

Though still in its early stages, the last few years have yielded rapid advances in our understanding of how the brain solves the input, output, and allocation control problems facing working memory. These experiments have associated all three functions with interactions between frontal and basal ganglia systems. Below, we review this work to outline an account of how the brain manages working memory.

Section snippets

From motor control to cognitive control

There is a clear parallel between the problems addressed by working memory control processes and the fundamental challenges faced by an animal's motor system. Consider the task of hunting for dinner. For example, a predator must program motor actions on the basis of transiently observed information about prey (input control); maintain these programs until the time is right, enacting only the most appropriate motor program at that time (output control); and finally, refrain from perseveratively

Input gating of working memory

Gating dynamics provide a powerful solution to the input control problem for working memory 6, 10, 12. When useful information becomes available in the environment, the gate is open and working memory is updated with this useful information. Otherwise, the gate is closed and irrelevant information is kept from needlessly occupying capacity.

Several computational models of working memory have achieved this gating dynamic using cortico-striatal mechanisms analogous to those described for the motor

Output gating of working memory

According to the prevailing top-down ‘biased competition’ model of prefrontal function, information residing in working memory actively biases behavior. However, not all information in working memory needs to be relevant at the same time, and indeed might cross-talk or mutually interfere if mere maintenance yielded an obligatory biasing influence. Clearly, the capacity to ‘single out’ or select relevant representations stored within working memory is adaptive [38]. Behavioral evidence indicates

Working memory content control: the case of reallocation

The rapidly developing literature on working memory input and output control has been strongly guided by the numerous models to posit that BG-mediated gating processes may address these problems. Unfortunately, computational models differ widely in how they treat a third kind of control problem. How is working memory reallocated when already-stored information is later revealed to be irrelevant? By some accounts, an active removal process is necessary; by others, passive decay could be

Conclusions

Working memory contends with the complexity of the real world via a set of control processes that select what items to maintain, which maintained items to use, and the priority of items within memory. Many of these demands are analogous to those faced in movement selection by the motor system. Accordingly, fronto-striatal mechanisms for motor selection might be elaborated in more rostral frontostriatal circuits and used for more abstract working memory operations. This long-held hypothesis has

Conflict of interest statement

Nothing declared.

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgements

This work was supported by awards from the National Institute of Neurological Disease and Stroke (R01 NS065046), the Alfred P. Sloan Foundation BR2011-010, and the James S. McDonnell Foundation 220020332. We also thank Michael Frank, Thomas Hazy, Seth Herd, Randy O’Reilly, and members of the Badre Lab for many valuable discussions on these topics.

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