Decoding the internal focus of attention
Highlights
► Distinct patterns of activity are associated with different domains of STM retention. ► These patterns are activated only when the STM item is in the focus of attention. ► Mass-univariate analysis and MVPA both dissociate attended and unattended STM items. ► Only MVPA reveals that unattended STM items are not actively maintained.
Introduction
Short-term memory refers to the ability to temporarily retain information when it is no longer present in the environment. The related and overlapping construct of working memory also incorporates the ability to manipulate or otherwise transform information, to protect it in the face of interference, and to use it to guide behavior. These abilities (from here on referred to as “STM”) are of central importance in the study of human cognition, being implicated as critical contributors to such functions and properties as language comprehension, learning, planning, reasoning and general fluid intelligence (Baddeley, 1986, Conway et al., 2003, Engle and Kane, 2003, Engle et al., 1999, Unsworth and Engle, 2007). The brain structures and cognitive processes underlying STM are topics of intense investigation and debate (see Jonides et al., 2008; and Postle, 2006b for reviews).
Many contemporary accounts of the neural bases of cognition (e.g., Haxby et al., 2001, Rogers and McClelland, 2004) describe mental representations as emergent properties of coordinated and distributed neural activity. However, many traditional techniques for analyzing neuroimaging data are poorly suited for the investigation of distributed systems. This is because they are limited to identifying magnitudes of activity in localized parts of the brain and, in effect, assume a homogeneity of representation within contiguous clusters of voxels. The profound importance of the recent introduction to cognitive neuroscience of multivariate pattern analysis (MVPA) (Haynes and Rees, 2006, Kriegeskorte et al., 2006, Norman et al., 2006, Pereira et al., 2009), therefore, is that it affords the detection and characterization of information that is represented in patterns of activity distributed within and across multiple regions of the brain.
The research that we present here is motivated by the embedded-component theories of STM (Cowan, 1988, Cowan, 1995, Ericsson and Kintsch, 1995, Oberauer, 2002), which characterize STM as an emergent property of the interaction of long-term memory and attention. They postulate a distinction between a capacity-limited central component of STM (referred to as the focus of attention) and a more peripheral component (outside the focus, commonly referred to as activated long-term memory). To date, we have leveraged MVPA to generate stronger neural evidence than had previously existed for the idea that reactivated long-term memory representations are the basis of STM (Lewis-Peacock & Postle, 2008), and to generate some of the first evidence (see also Nee and Jonides, 2008, Nee and Jonides, 2011) that the distinction between attended and unattended representations within STM, which has been proposed on the basis of behavioral evidence (Cowan, 1988, Oberauer, 2002), has a neural basis (Lewis-Peacock et al., in press). Independent of the embedded-component model, the results from this latter study have demonstrated that the active neural signature of information being remembered across a brief delay can be disrupted by redirecting attention, without sacrificing the short-term retention of that information. This finding raises questions about the common view in cognitive neuroscience that the maintenance of persistently elevated neural activity is required for the short-term retention of information, and supports an alternative model: the sustained activation of a stimulus representation is not necessary for its short-term retention; this activity, instead, corresponds to the focus of attention.
Here, we present several additional analyses of the data from Lewis-Peacock et al. (in press) that compare the inferences that can be drawn from MVPA vs. from univariate approaches based on the general linear model (GLM). We began by attempting to decode brain activity, not from multivariate patterns of activity throughout the brain, but from the average activity inside category-selective regions of interest (ROI). The successes and failures of this approach in replicating the results from MVPA are instructive. The successes provide confirmatory evidence that neural representations inside and outside the focus of attention are neurally dissociable. The failures of the GLM approach, however, illustrate how MVPA can provide additional insights into the neural bases of cognition. For example, MVPA alone was able to verify that STM representations, like perceptual ones (Haxby et al., 2001), are widely distributed and overlapping, and that they can be observed in brain regions which fail to show elevated activity during the delay period (e.g., Serences et al., 2009, Harrison and Tong, 2009). Also, the multivariate results highlight potentially misleading interpretations of univariate results (e.g., Postle, 2006a) that are based on the (faulty) assumption of homogeneity of representation in category-selective brain regions.
Section snippets
Behavioral task
A full description of the design and analysis of this experiment is presented in Lewis-Peacock et al. (in press). Here, we provide a brief overview. Nine healthy young adults were scanned in one session performing two different tasks. In the first, they performed short-term recognition of a stimulus drawn from one of three categories: words, pronounceable pseudo-words, or line segments (Fig. 1, Phase 1). Subjects indicated whether the probe stimulus matched the target stimulus (p = 0.5) according
Behavior
Full behavioral results for the Phase 1 and Phase 2 tasks are reported in Lewis-Peacock et al. (in press). The mean accuracy and response time across all participants in the Phase 1 task were 94% (SEM = 1) and 933 ms (SEM = 22). The mean accuracy and response time across all participants in the Phase 2 task were 91% (SEM = 1) and 936 ms (SEM = 10). Participants were more accurate (F(1,8) = 27.18, p < 0.001) and faster to respond (F(1,8) = 7.86, p = 0.023) on repeat trials (93%, SEM = 1; 898 ms, SEM = 13) than on
Discussion
Our recent findings (Lewis-Peacock et al., in press) derived with MVPA, have provided some of the first neural evidence for a distinction between attended and unattended representations in STM, and they have also revealed a novel insight: the active neural signature of information being remembered across a brief delay can be disrupted by redirecting attention, without sacrificing the short-term retention of that information. This finding raises questions about the common view in cognitive
Acknowledgements
This work was supported by National Institutes of Health Grant MH064498 (BRP) and MH085444 (JALP). We want to thank Klaus Oberauer and Andrew Drysdale for their helpful contributions to the design of the experiment analyzed here, the original MVPA analysis of which was reported in Lewis-Peacock et al. (in press).
References (65)
- et al.
Human memory: A proposed system and its control processes
The Psychology of Learning and Motivation: Advances in Research and Theory
(1968) - et al.
A revised model of short-term memory and long-term learning of verbal sequences
Journal of Memory and Language
(2006) - et al.
Working memory capacity and its relation to general intelligence
Trends in Cognitive Sciences
(2003) - et al.
Functional magnetic resonance imaging (fMRI) “brain reading”: Detecting and classifying distributed patterns of fMRI activity in human visual cortex
Neuroimage
(2003) - et al.
Persistent activity in the prefrontal cortex during working memory
Trends in Cognitive Sciences
(2003) - et al.
A distributed representation of temporal context
Journal of Mathematical Psychology
(2002) - et al.
An event-related fMRI investigation of phonological versus semantic short-term memory
Journal of Neurolinguistics
(2003) - et al.
Transcranial magnetic stimulation of medial prefrontal cortex modulates face expressions processing in a priming task
Neuropsychologia
(2011) Accessing recent events
Psychology of Learning and Motivation
(2006)- et al.
Dissociable contributions of prefrontal cortex and the hippocampus to short-term memory: Evidence for a 3-state model of memory
Neuroimage
(2011)
Beyond mind-reading: Multi-Voxel pattern analysis of fMRI data
Trends in Cognitive Sciences
Machine learning classifiers and fMRI: A tutorial overview
Neuroimage
Distraction-spanning sustained activity during delayed recognition of locations
Neuroimage
Working memory as an emergent property of the mind and brain
Neuroscience
Analysis of fMRI time-series revisited—Again
Neuroimage
Working memory
Short-Term memory for serial order: A recurrent neural network model
Psychological Review
The search for the phonological store: From loop to convolution
Journal of Cognitive Neuroscience
Memory for serial order: A network model of the phonological loop and its timing
Psychological Review
Long-Term memory is the representational basis for semantic verbal short-term memory
Psychophysiology
Patterns of activity in the categorical representations of objects
Journal of Cognitive Neuroscience
Are face-responsive regions selective only for faces?
Neuroreport
Evovling conceptions of memory storage, selective attention, and their mutual constraints within the human information-processing system
Psychological Bulletin
Attention and memory: An integrated framework
The magical number 4 in short-term memory: A reconsideration of mental storage capacity (vol. 23, p. 87, 2001)
Behavioral and Brain Sciences
Removing irrelevant information from working memory: Domain-Specific prioritization takes time
Pattern classification
Executive attention, working memory capacity, and a two-factor theory of cognitive control
Psychology of learning and motivation
Individual differences in working memory capacity and what they tell us about controlled attention, general fluid intelligence, and functions of the prefrontal cortex
Long-term working memory
Psychological Review
An endogenous distributed model of ordering in serial recall
Psychonomic Bulletin & Review
Neuron activity related to short-term memory
Science
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