Trends in Cognitive Sciences
ReviewRevisiting the role of persistent neural activity during working memory
Introduction
WM comprises the set of operations that support the active retention of behaviorally relevant information over brief intervals. Given the central role of WM in goal-directed behavior, establishing the neural basis of WM has been a priority of neuroscience research. Early WM studies observed that selective increases in neural activity during the presentation of a to-be-maintained sample item persisted throughout the blank ‘delay’ interval of a WM delay task, bridging the temporal gap between the sample and the subsequent contingent response 1, 2. This work inspired the theoretical framework that has predominated in the field: neurons or neuronal populations that are selectively tuned to the to-be-remembered information hold this information in an active state through persistent activation [3]. We refer to this model, which emphasizes stable persistent neural activity (see Glossary) in selective neurons as the fixed-selectivity model. Motivated by this model, functional MRI (fMRI) studies in humans and electrophysiological studies in monkeys have consistently identified persistent neural activity in the lPFC, leading many to conclude that the lPFC stores representations of WM memoranda.
A decade ago, we provided a critique of the literature on persistent activity in the context of contemporary models of prefrontal cortical function [4]. We hypothesized that, in contrast to existing theories of WM, persistent lPFC activity signifies attention directed to internal representations maintained in sensory cortices. Viewed through the lens of the fixed-selectivity model, evidence for this proposal is limited. Studies of sensory and motor function, however, suggest that information is likely to be represented through the combined activity of neural populations with diverse tuning properties rather than individual highly-tuned neurons 5, 6. This notion offers a promising framework for understanding WM.
In recent years, analytic and methodological advances (Box 1) have expanded researchers’ ability to capture the multivariate nature of population coding and the causal relationships between neural activity and behavior. The findings generated using these approaches underscore the need for a revision of existing views of WM. In light of these results, we revisit the issue of how information remains active during WM. The studies we discuss here focus on visual WM, but the general principles discussed herein apply to WM in other modalities.
Section snippets
Evidence for persistent WM representations in visual cortex
Neurons in visual cortex are selectively tuned to visual stimulus features and are consequently well suited for maintaining high-fidelity representations of visual information in the service of WM [7]. Yet, from the perspective of the fixed-selectivity model, evidence for sustained WM representations in visual cortex has been equivocal. Although sustained responses have been observed in temporal cortex [8], studies typically describe transient neural responses to sample stimuli without any
The role of the lPFC in WM
The most pervasive observation in the WM literature is that lPFC activity persists throughout WM maintenance. This finding has been interpreted as evidence that lPFC delay activity encodes sensory features of WM items [3]. However, in addition to displaying coarse selectivity for WM items and features [33], lPFC activity exhibits selectivity for a broad range of task variables during the delay period of WM tasks. For example, lPFC neurons show differential preferences for task rules [34],
Persistent neural activity revisited
Persistent neural activity, particularly in the lPFC, has become synonymous with WM. However, this equivalence is misleading. First, the lPFC does not appear to be privileged in its ability to generate persistent activity. Particularly when analyses focus on neurons or voxels that are highly stimulus selective, persistent neural activity can be observed nearly everywhere in the brain 8, 64, 65, 66. Second, although persistent neural activity is a key mechanism for forming temporal links between
Concluding remarks
An understanding of the neural mechanisms underlying WM is critical for gaining insight into the wide range of goal-directed behaviors supported by WM. In this review, we present a perspective on WM that emphasizes the notion of distributed population activity in encoding WM information. Methodological advances in the past ten years, and in the past few years in particular, have highlighted the sensory nature of sustained WM information in sensory cortices and the high-dimensional nature of
Acknowledgments
This work was supported by grants from the National Institutes of Health (R01 MH63901 to M.D. and R01 EY016407 and R03 MH097206 to C.E.C.).
Glossary
- Delay tasks
- the experimental paradigm typically used to study the neural basis of working memory (WM). A trial in a delay task begins with a brief presentation of a sample item. The subject encodes this item into WM and maintains this item over a blank ‘delay’ period of a few to several seconds. At the end of the delay period, a probe stimulus appears and the subject initiates a behavioral response contingent on the WM representation of the sample item. A key feature of delay tasks is that they
References (96)
Cellular basis of working memory
Neuron
(1995)- et al.
Persistent activity in the prefrontal cortex during working memory
Trends Cogn. Sci.
(2003) - et al.
Directing the mind's eye: prefrontal, inferior and medial temporal mechanisms for visual working memory
Curr. Opin. Neurobiol.
(2005) The role of early visual cortex in visual short-term memory and visual attention
Vision Res.
(2009)Beyond mind-reading: multi-voxel pattern analysis of fMRI data
Trends Cogn. Sci.
(2006)Shared representations for working memory and mental imagery in early visual cortex
Curr. Biol.
(2013)Multi-voxel pattern analysis of selective representation of visual working memory in ventral temporal and occipital regions
Neuroimage
(2013)- et al.
Visual working memory capacity: from psychophysics and neurobiology to individual differences
Trends Cogn. Sci.
(2013) Dynamic coding for cognitive control in prefrontal cortex
Neuron
(2013)- et al.
Generating coherent patterns of activity from chaotic neural networks
Neuron
(2009)
Working memory as an emergent property of the mind and brain
Neuroscience
Goal-directed attention alters the tuning of object-based representations in extrastriate cortex
Front. Hum. Neurosci.
The prefrontal cortex – an update: time is of the essence
Neuron
Concurrent brain-stimulation and neuroimaging for studies of cognition
Trends Cogn. Sci.
Beyond working memory: the role of persistent activity in decision making
Trends Cogn. Sci.
Brain mechanisms for perceptual and reward-related decision-making
Prog. Neurobiol.
Single-trial neural correlates of arm movement preparation
Neuron
Neuronal circuits underlying persistent representations despite time varying activity
Curr. Biol.
Analyses of regional-average activation and multivoxel pattern information tell complementary stories
Neuropsychologia
Confounds in multivariate pattern analysis: theory and rule representation case study
Neuroimage
Computational advances towards linking BOLD and behavior
Neuropsychologia
Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research
Clin. Neurophysiol.
The functional role of cross-frequency coupling
Trends Cogn. Sci.
Direct brain recordings fuel advances in cognitive electrophysiology
Trends Cogn. Sci.
Large-scale brain networks in cognition: emerging methods and principles
Trends Cogn. Sci.
Neuron activity related to short-term memory
Science
Mnemonic coding of visual space in the monkey's dorsolateral prefrontal cortex
J. Neurophysiol.
Neuronal population coding of movement direction
Science
Decoding the activity of neuronal populations in macaque primary visual cortex
Nat. Neurosci.
Working memory in primate sensory systems
Nat. Rev. Neurosci.
Pattern Classification
Fast readout of object identity from macaque inferior temporal cortex
Science
Decoding patterns of human brain activity
Annu. Rev. Psychol.
Decoding and reconstructing color from responses in human visual cortex
J. Neurosci.
Decoding reveals the contents of visual working memory in early visual areas
Nature
Stimulus-specific delay activity in human primary visual cortex
Psychol. Sci.
A neural measure of precision in visual working memory
J. Cogn. Neurosci.
Decoding working memory of stimulus contrast in early visual cortex
J. Neurosci.
Mapping brain activation and information during category-specific visual working memory
J. Neurophysiol.
Decoding the contents of visual short-term memory from human visual and parietal cortex
J. Neurosci.
Neural dynamics in inferior temporal cortex during a visual working memory task
J. Neurosci.
Distributed and dynamic storage of working memory stimulus information in extrastriate cortex
J. Cogn. Neurosci.
The relationship between working memory storage and elevated activity as measured with functional magnetic resonance imaging
J. Neurosci.
Neural measures reveal individual differences in controlling access to working memory
Nature
Basing perceptual decisions on the most informative sensory neurons
J. Neurophysiol.
Distributed patterns of activity in sensory cortex reflect the precision of multiple items maintained in visual short-term memory
J. Neurosci.
Topographic contribution of early visual cortex to short-term memory consolidation: a transcranial magnetic stimulation study
J. Neurosci.
Causal evidence for subliminal percept-to-memory interference in early visual cortex
Neuroimage
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