Review
The Distributed Nature of Working Memory

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There is no evidence for a single site of working memory storage. Rather, persistent neuronal activity that is informative about a currently memorized stimulus can be found in sensory, parietal, and prefrontal brain regions.

Working memory entails a gradient of abstraction from sensory areas reflecting low-level sensory features to prefrontal regions encoding more abstract, semantic, and response-related aspects of stimuli.

We hypothesize that all regions of neocortex have the capability to briefly retain their specialized representations in the service of upcoming task demands. Persistent activity in most, if not all, cortical regions can exert control over future behavior.

The contributions of individual brain regions to working memory are best understood as different representational stages with various levels of transformation and abstraction.

Studies in humans and non-human primates have provided evidence for storage of working memory contents in multiple regions ranging from sensory to parietal and prefrontal cortex. We discuss potential explanations for these distributed representations: (i) features in sensory regions versus prefrontal cortex differ in the level of abstractness and generalizability; and (ii) features in prefrontal cortex reflect representations that are transformed for guidance of upcoming behavioral actions. We propose that the propensity to produce persistent activity is a general feature of cortical networks. Future studies may have to shift focus from asking where working memory can be observed in the brain to how a range of specialized brain areas together transform sensory information into a delayed behavioral response.

Section snippets

Storage of Working Memory Contents

Cognition critically depends on the ability to memorize information and change it adaptively. This ability is typically ascribed to working memory, which has often been conceptualized as comprising two basic functions: (i) short-term storage of information and (ii) executive processes that retain no information themselves but control what is retained 1, 2. Here, we argue that instead of being discrete, these functions could be considered extreme functional specializations of a distributed

Why Are Working Memory Representations Distributed?

The presence of working memory signals in both low-level and high-level cortices suggests some kind of distributed representation (Box 1). There are several accounts for this finding (Figure 2). For example, it could in theory reflect a full duplication of sensory information in the PFC (Figure 2A; [8]). While the redundancy of such duplicate representations might, at first sight, stand in contradiction to evolutionary frugality 4, 5, it could be useful in establishing the robustness of working

A Working Memory Gradient

We conceptualize working memory as a hierarchical process that links detailed sensory representations to specific behavioral responses via intermediate task-relevant representations and action plans in a network of brain areas that each represent the working memory in a format that matches their functional specialization (see also [15]). Thus, we propose that every cortical region can produce persistent stimulus-selective activity if the features that are coded in that region need to be

Concluding Remarks

There is abundant evidence for widely distributed stimulus-related information in sensory, parietal, and prefrontal cortices during working memory delays. In the absence of evidence implicating any of these regions as an exclusive and localized store of memory contents, we suggest that working memory is better characterized as a distributed network that gradually transforms sensory information towards an appropriate behavioral response, across a temporal delay. Persistent stimulus-specific

Acknowledgments

The authors would like to thank Ilja G. Sligte for helpful discussion. TBC & JDH were supported by the Bernstein Computational Neuroscience Program of the German Federal Ministry of Education and Research (grant reference 01GQ1001C); the Deutsche Forschungsgemeinschaft (DFG) grants SFB 940, Neurocure (Exc 257), KFO247, and German-Israeli Project Cooperation DIP (JA 945/3-1); and the European Regional Development Funds (grant references 10153458 and 10153460). PCK is supported by VENI grant

Glossary

Abstract representation
high-level representation of memorized stimuli that is less detailed with regards to specific physical stimulus features, but that allows for generalization across a large number of stimuli that share the same semantic property or that belong to the same category.
Activity-silent working memory
neural mechanisms of working memory that are not directly detectable as changes in spike rate (or BOLD activity), for example: temporary changes in synaptic efficacy.
Distributed

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    These authors contributed equally to this work.

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