Review
Top-down modulation: bridging selective attention and working memory

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Selective attention, the ability to focus our cognitive resources on information relevant to our goals, influences working memory (WM) performance. Indeed, attention and working memory are increasingly viewed as overlapping constructs. Here, we review recent evidence from human neurophysiological studies demonstrating that top-down modulation serves as a common neural mechanism underlying these two cognitive operations. The core features include activity modulation in stimulus-selective sensory cortices with concurrent engagement of prefrontal and parietal control regions that function as sources of top-down signals. Notably, top-down modulation is engaged during both stimulus-present and stimulus-absent stages of WM tasks; that is, expectation of an ensuing stimulus to be remembered, selection and encoding of stimuli, maintenance of relevant information in mind and memory retrieval.

Section snippets

Top-down modulation in perception and working memory

Selective attention and working memory (WM) have traditionally been viewed as distinct cognitive domains (see Glossary). However, a growing number of psychological and neuroscientific studies have revealed extensive overlap between these two constructs, spurring a number of excellent reviews and theoretical discussions on this topic 1, 2, 3, 4, 5. In this review, we focus on recent neural evidence highlighting how top-down modulatory mechanisms, similar to those described for selective

Expectation

Expectations of upcoming events generated by predictive cues enhance perceptual performance, notably improving the speed and accuracy of stimulus detection and discrimination [10]. The neural basis of this phenomenon has been most frequently studied using perceptual tasks, and is characterized by stimulus-absent, top-down modulation of neural activity in sensory cortices before stimulus presentation. For example, pre-stimulus enhancement has been demonstrated in visual cortices following

Encoding

The differential modulation of activity in sensory cortices by attention to relevant versus irrelevant stimuli during WM encoding has been shown to be comparable to activity modulation generated in purely perceptual tasks. Goal-related influences occur at both early and late phases of stimulus processing [26] in stimulus-selective sensory cortices 27, 28. There is now accumulating support for a direct relationship between early goal-driven activity modulation in sensory areas (within 200 ms of

Maintenance

Encoding into WM was traditionally considered to be the end point of selective attention. Early seminal work showed that retrieval of items from a previously presented array could be improved only by selective spatial retrieval cues (post-cues) appearing after very brief intervals, when representations were thought to exist in a rapidly decaying photographic ‘iconic’ format. Post-cues became ineffective shortly afterward, during WM maintenance 38, 39, 40. Once encoded, WM representations were

Retrieval

Given the multiple stages of the delayed-recognition task at which top-down modulation can influence WM performance, finally we must ask whether the retrieval process itself is influenced by these mechanisms. This issue seems to have undergone little direct investigation. Conceptual as well as pragmatic issues may make the question difficult to tackle. For example, it is difficult to separate effects operating at retrieval from the cascading consequences of effects that have accrued during

Concluding remarks

We conclude that the neural mechanism of top-down modulation serves as a common framework for selective attention processes in the service of both perceptual goals and those that underlie the different stages of WM operations (Box 2). Top-down modulation of information processing appears analogous between these constructs, in terms of both the site of activity modulation in the sensory cortices and the putative sources of top-down signals originating from cortical control areas. We propose that

Acknowledgements

This work was supported by the National Institutes of Health R01-AG030395 (AG), the American Federation of Aging Research (AG), the Ellison Medical Foundation (AG), the James S. McDonnell Foundation (ACN) and the Wellcome Trust (ACN).

Glossary

Selective attention
goal-directed focus on one aspect of the environment, while ignoring irrelevant aspects.
Working memory
maintenance and/or manipulation of task-relevant information in mind for brief periods of time to guide subsequent behavior.
Delay-response tasks
a commonly used cognitive paradigm to study working memory. It is particularly valuable for use in neural studies, because the stages of working memory can be dissociated in time: expectation, encoding, maintenance and retrieval.

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