Elsevier

Acta Psychologica

Volume 132, Issue 2, October 2009, Pages 106-114
Acta Psychologica

Interactions between working memory, attention and eye movements

https://doi.org/10.1016/j.actpsy.2009.01.005Get rights and content

Abstract

This paper reviews the recent findings on working memory, attention and eye movements. We discuss the research that shows that many phenomena related to visual attention taking place when selecting relevant information from the environment are similar to processes needed to keep information active in working memory. We discuss new data that show that when retrieving information from working memory, people may allocate visual spatial attention to the empty location in space that used to contain the information that has to be retrieved. Moreover, we show that maintaining a location in working memory not only may involve attention rehearsal, but might also recruit the oculomotor system. Recent findings seem to suggest that remembering a location may involve attention-based rehearsal in higher brain areas, while at the same time there is inhibition of specific motor programs at lower brain areas. We discuss the possibility that working memory functions do not reside at a special area in the brain, but emerge from the selective recruitment of brain areas that are typically involved in spatial attention and motor control.

Introduction

In every-day life we often make use of our ability to temporarily store information until our task is completed. Working memory – which refers to the process of actively maintaining relevant information in mind for brief periods of time – is thought to underlie this ability. One of the most influential conceptualizations of working memory is the multiple component model of Baddeley and colleagues (e.g., Baddeley, 1986, Baddeley and Hitch, 1974). In the original model, Baddeley and colleagues suggested two independent buffers for the storage of verbal and visuospatial information. In a later version of the model, an additional buffer was added called “episodic buffer” which was assumed to link information across domains to form integrated units of visual, spatial, and verbal information (Baddeley, 2000). The Central Executive makes it possible to manage information in and between the different buffers. The present paper focuses on the visuospatial aspect of working memory. It refers to the process that allows retention and manipulation of information that is no longer available in the environment.

While it is possible to direct attention to information that is held in working memory, it is also possible to direct attention to relevant information that is still present in the environment. A long line of research has demonstrated that the allocation of visual attention to locations in visual space results in enhancement of processing of information that is presented at the attended location on both behavioral and neural levels (Mangun et al., 2001, Munneke et al., 2008, Peelen et al., 2004, Posner, 1980).

Recent work by Awh and colleagues (Awh and Jonides, 2001, Awh et al., 1998) indicates that, at least for visuospatial memory, there is a close link between working memory and visual attention. They showed that when a location is kept in working memory, processing of stimuli at the memorized location is facilitated relative to other locations (Awh & Jonides, 2001), just like attending to a location improves the processing of information at that location (Posner, 1980). Conversely, when attention to memorized locations is interrupted, the ability to remember these locations is impaired (Awh et al., 1998). Brain imaging studies of working memory confirm the notion that rehearsal of spatial information modulates early sensory areas (Awh et al., 1999), and that the same fronto-parietal network is involved as in attention-related tasks (Kastner & Ungerleider, 2000).

In the present paper, we review the recent findings on working memory and attention. We mainly focus on the research from our own laboratory. We discuss the relationship between the allocation of visual attention and working memory. We show that many phenomena related to visual attention taking place when selecting relevant information from the environment also occur when those stimuli are kept active in working memory. We show that maintaining a location in working memory not only may involve attention rehearsal, but also may recruit the oculomotor system. We discuss some recent findings suggesting that remembering a location may involve attention-based rehearsal in higher brain areas, while at the same time there is inhibition of specific motor programs at lower brain areas. We discuss the possibility that working memory functions do not reside at a special area in the brain, but emerge from the selective recruitment of brain areas that are typically involved in spatial attention and motor control, a view consistent with the notion of Grounded Cognition (e.g., Barsalou, 2008).

Section snippets

Working memory and attention

As a metaphor visual attention has been compared to a spotlight that “selects” parts of the visual world around us (e.g., Posner, 1980). Visual attention allows people to select information that is relevant for their ongoing behavior. Providing information about the location of an upcoming target usually involves a cueing procedure in which a cue indicates with a high probability (e.g., in 80% trials the information provided to the participant is valid) the location of the upcoming target. Such

Working memory and eye movements

As described above, there appears to be a strong link between visual working memory and attention. In turn, an equally strong link exists between spatial attention and eye movements. Previous research has shown that the eyes typically move to the location where attention is allocated, and, vice versa, attention is allocated at possible saccade targets (Deubel and Schneider, 1996, Hoffman and Subramaniam, 1995, Kowler et al., 1995).

In a study conducted in our laboratory, we showed that just

Discussion

In this paper, we discussed evidence suggesting a strong overlap between visual working memory, spatial attention and the oculomotor system. The premotor theory of attention (Rizzolatti et al., 1987, Sheliga et al., 1994) provides a framework to explain the strong overlap. According to this theory, the activation of neural structures related to attention depends on the required motor action. Thus, spatial attention shifts are considered to be a byproduct of preparing a saccadic eye movement, or

Acknowledgement

Correspondence concerning this article should be addressed to Jan Theeuwes, Dept. of Cognitive Psychology, Vrije Universiteit, van der Boechorststraat 1, 1081 BT Amsterdam, The Netherlands. Electronic mail may be sent to [email protected]. This research was funded by a grant from NWO (Netherlands organization for Scientific Research), grant to JT and NWO-Vidi grant 452-06-007 to C.N.L.O.

References (77)

  • G.R. Mangun et al.

    Integrating electrophysiology and neuroimaging of spatial selective attention to simple isolated visual stimuli

    Vision Research

    (2001)
  • J. Munneke et al.

    Directing attention to a location in space results in retinotopic activation in primary visual cortex

    Brian Research

    (2008)
  • M.V. Peelen et al.

    Endogenous and exogenous attention shifts are mediated by the same large-scale neural network

    Neuroimage

    (2004)
  • B.R. Postle

    Working memory as an emergent property of the mind and brain

    Neuroscience

    (2006)
  • G. Repovs et al.

    The multi-component model of working memory: Explorations in experimental cognitive psychology

    Neuroscience

    (2006)
  • G. Rizzolatti et al.

    Reorienting attention across the horizontal and vertical meridians: Evidence in favor of a premotor theory of attention

    Neuropsychologia

    (1987)
  • J. Theeuwes

    Effects of location and form cuing on the allocation of attention in the visual field

    Acta Psychologica

    (1989)
  • J. Theeuwes et al.

    Inhibition of return and oculomotor interference

    Vision Research

    (2004)
  • S. Van der Stigchel et al.

    Eye movement trajectories and what they tell us

    Neuroscience & Biobehavioral Reviews

    (2006)
  • H. Aizawa et al.

    Reversible inactivation of monkey superior colliculus I. Curvature of saccadic trajectory

    Journal of Neurophysiology

    (1998)
  • E. Awh et al.

    Human rehearsal processes and the frontal lobes: PET evidence

  • E. Awh et al.

    Rehearsal in spatial working memory

    Journal of Experimental Psychology-Human Perception and Performance

    (1998)
  • E. Awh et al.

    Rehearsal in spatial working memory: Evidence from neuroimaging

    Psychological Science

    (1999)
  • A.D. Baddeley

    Working memory

    (1986)
  • A.D. Baddeley et al.

    Spatial working memory

  • L.W. Barsalou

    Grounded cognition

    Annual Review of Psychology

    (2008)
  • A.V. Belopolsky et al.

    Transfer of information into working memory during attentional capture

    Visual Cognition

    (2008)
  • Belopolsky, A.W., & Theeuwes., J. (in press). Inhibition of saccadic eye movements to locations in spatial working...
  • J.W. Bisley et al.

    Neuronal activity in the lateral intraparietal area and spatial attention

    Science

    (2003)
  • C. Bundesen

    A theory of visual attention

    Psychological Review

    (1990)
  • L. Chelazzi et al.

    Cortical mechanisms of visuospatial attention in the primate brain

  • A.B. Chica et al.

    Dissociating inhibition of return from endogenous orienting of spatial attention: Evidence from detection and discrimination tasks

    Cognitive Neuropsychology

    (2006)
  • S.M. Courtney et al.

    An area specialized for spatial working memory in human frontal cortex

    Science

    (1998)
  • M. Doyle et al.

    Curved saccade trajectories: Voluntary and reflexive saccades curve away from irrelevant distractors

    Experimental Brain Research

    (2001)
  • P.E. Downing et al.

    Competition in visual working memory for control of search

    Visual Cognition

    (2004)
  • J. Duncan et al.

    Visual search and stimulus similarity

    Psychological Review

    (1989)
  • M.J. Farah

    Psychophysical evidence for shared representational medium for mental images and percepts

    Journal of Experimental Psychology: General

    (1985)
  • R. Godijn et al.

    Programming of endogenous and exogenous saccades: Evidence for a competitive integration model

    Journal of Experimental Psychology: Human Perception and Performance

    (2002)
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