Elsevier

Neuropsychologia

Volume 49, Issue 12, October 2011, Pages 3303-3313
Neuropsychologia

Attention and the readiness for action

https://doi.org/10.1016/j.neuropsychologia.2011.08.003Get rights and content

Abstract

The initiation of voluntary action is preceded by up to 2 s of preparatory neural activity, originating in premotor and supplementary motor regions of the brain. The function of this extended period of pre-movement activity is unclear. Although recent studies have suggested that pre-movement activity is influenced by attention to action, little is understood about the specific processes that are involved in this preparatory period prior to voluntary action. We recorded readiness potentials averaged from EEG activity as participants made voluntary self-paced finger movements. We manipulated the processing resources available for action preparation using concurrent perceptual load and cognitive working memory load tasks. Results showed that pre-movement activity was significantly reduced only under conditions of high working memory load, when resources for planning action were limited by the concurrent cognitive load task. In contrast, limiting attentional resources in the perceptual load task had no effect on pre-movement readiness activity. This suggests that movement preparatory processes involve mechanisms of cognitive control that are also required for working memory, and not more general engagement of selective attentional resources. We propose that the extended period of pre-movement neural activity preceding voluntary action reflects the engagement of cognitive control mechanisms for endogenously orienting attention in time, in readiness for the initiation of voluntary action.

Highlights

► We examined the role of attention in neural activity preceding voluntary movement. ► We varied perceptual and cognitive working memory load during self-paced actions. ► Early, centralized pre-movement activity was reduced under high cognitive load. ► Limiting attention via perceptual load had no effect on pre-movement activity. ► Action preparation relies on cognitive resources rather than general attention.

Introduction

Voluntary movements are planned and represented in the brain before they are initiated. Functional magnetic resonance imaging (fMRI) suggests a crucial role for the supplementary motor area (SMA) in the preparation for voluntary action, with activity in this region consistently shown to precede activity of the primary motor cortex prior to the initiation of movement (Ball et al., 1999, Cunnington et al., 2003, Cunnington et al., 2005, Wildgruber et al., 1997), a finding that has been replicated by studies using positron emission tomography (PET) (MacKinnon et al., 1996) and magnetoencephalography (MEG) (Erdler et al., 2000). Electroencephalographic (EEG) studies of the slow, negative, scalp-recorded potential known as the Bereitschaftspotential, or readiness potential (Kornhuber & Deecke, 1965), suggest that this preparatory activity begins up to 2 s prior to voluntary action.

While this pre-movement neural activity is considered to represent movement-specific planning of factors such as movement direction (Cui & Deecke, 1999), body part (Boschert and Deecke, 1986, Kitamura et al., 1993), force (Becker & Kristeva, 1980), and speed (Becker, Iwase, Jurgens, & Kornhuber, 1976), its precise function over such an extended time scale prior to movement is unclear. The earliest component of pre-movement activity of the readiness potential, beginning up to 2 s prior to movement, is characterized by a slowly increasing negativity, maximal over the vertex (Shibasaki & Hallett, 2006), and is thought to reflect activity predominantly in the SMA, pre-SMA, and anterior cingulate motor areas (Ball et al., 1999, Cunnington et al., 2005). Later stage movement-specific planning and execution is thought to be reflected in the late component of the readiness potential, beginning approximately 500 ms before movement and with maximal amplitude over the motor cortex contralateral to the moving limb (Deecke, Scheid, & Kornhuber, 1969).

The function of this very early pre-movement neural activity is not clear. When responding or reacting to external stimuli, complex movements can be performed with very little preparation time if necessary, thus obligatory motor planning processes alone cannot account for such an early and long period of cortical activity preceding movement. Non-motor processes such as motivation to move (McAdam & Seales, 1969), intentional involvement (Kornhuber & Deecke, 1965), awareness of movement (Keller & Heckhausen, 1990), spontaneity (Libet et al., 1982, McArdle et al., 2009), and freedom of movement selection (Dirnberger et al., 1998, Praamstra et al., 1995), have been implicated as factors involved in early pre-movement activity. Neuroimaging studies have shown movement-related brain activity to be strongly modulated by the level of attention and intention involved in the movement (Lau, Rogers, Haggard, & Passingham, 2004). Anterior cingulate, prefrontal and premotor areas, including the SMA, are more active when attending to a movement being performed than when performing it automatically (Jueptner et al., 1997, Passingham, 1996, Rowe et al., 2002) or when attention is occupied by a distractor task (Johansen-Berg & Matthews, 2002). Lau et al. (2004) found that activity in the pre-SMA was greater when participants attended to their intention to move, rather than to the action itself. This suggests that increased attentional and intentional involvement engages the higher motor areas involved in pre-movement planning, and that activity in the SMA in particular may represent intentional or cognitive processes that are strongly influenced by attention.

Attention, however, is not a unitary process, and the precise processes that contribute to early pre-movement preparatory activity therefore remain unclear. In this study, we compared how the engagement of selective attentional resources in a perceptual task and the engagement of cognitive resources involved in working memory each influence early pre-movement activity prior to voluntary action. While most previous studies of attention to action relied on instructing participants to direct attention towards particular aspects of their movement, here we used a dual-task paradigm in which two competing tasks were performed simultaneously. This is a well-controlled method for manipulating and examining effects of limited-capacity resources on a given task (Fisk et al., 1986, Wickens, 1984). By combining a voluntary movement task with a secondary task in which the relative difficulty or “load” was varied parametrically, we could limit the degree to which resources could be allocated or engaged in the preparation for voluntary action.

Additionally, by comparing the effects of perceptual and cognitive load tasks, we were able to elucidate the specific processes involved during the early period of movement preparation. Our perceptual load task involved the detection of pre-specified target letters amongst a rapid sequential stream of distractor letters, with load manipulated by increasing the visual similarity of target and distractor letters, thereby engaging limited-capacity selection processes. The cognitive load task was a version of the n-back task, in which participants were presented with a stream of letters and were required to match the current stimulus with the one presented up to two items ago, thereby placing substantial demands on working memory (Owen, McMillan, Laird, & Bullmore, 2005). In a broad sense, both perceptual and cognitive load tasks could be considered to load attention, in that both limit the degree to which participants can attend or allocate resources to the planning for action. However, perceptual and cognitive load tasks are also likely to draw on different neural resources, based on the theory that there exist specialized and separable attentional processing modules (Allport, 1980, Wickens, 1980).

Crucially, to ensure that the load manipulations engaged processing resources in both tasks, we conducted a behavioral validation study, independent of the readiness potential experiments. While performing either the perceptual or cognitive load task, we measured participants’ response times to detect occasional brief dot stimuli presented unpredictably on the left or right of the screen. This type of probe task is typically used as an index of processing demands amongst multiple tasks (Posner & Boies, 1971). Speed and accuracy of responses to the dot probes provide a measure of the extent to which processing resources are loaded by the secondary tasks (Fisk et al., 1986), thus indicating the effectiveness of our load manipulations.

While previous studies of attention to action have generally used fMRI, by using EEG to examine readiness potentials preceding movement initiation we were better able to distinguish the time periods during movement planning that are most influenced by attention to action. In particular, we aimed to examine the effect of attentional load on the earliest component of pre-movement activity beginning up to 2 s prior to movement. It is this component that is thought to reflect activity predominantly in the SMA, pre-SMA, and anterior cingulate motor areas (Ball et al., 1999, Cunnington et al., 2005), and it is this early period of pre-movement activity that appears to be most affected by Parkinson's disease (Cunnington, Iansek, Johnson, & Bradshaw, 1997).

Therefore, by examining pre-movement activity in the readiness potential prior to voluntary finger movement as participants performed the different load tasks, we aimed to determine how the engagement of selective attentional resources (as indexed by the perceptual attention task), or cognitive resources (as indexed by the working memory task), influence the early processes that precede the initiation of voluntary movement. If the planning for action, and corresponding pre-movement neural activity, relies on the engagement of selective attentional or cognitive resources, we would expect readiness potential amplitudes to be reduced with increasing load in the perceptual or cognitive load tasks.

Section snippets

Participants

Three independent groups of participants were recruited: two groups for the studies of perceptual and cognitive load on pre-movement neural activity in the readiness potential, and a further group for the behavioral validation study of the load tasks. All participants were right-handed and all had normal or corrected-to-normal vision. All studies were approved by the relevant local human research ethics committees.

Eighteen healthy volunteers (8 male, 10 female) aged between 21 and 29 years

Task performance

Performance on the load tasks, for both perceptual and cognitive load, are displayed in Fig. 2a. Target letter accuracy was found to be significantly higher in the low-load condition compared to the high-load condition, in both the perceptual load task, t(15) = 6.89, p < .001, and the cognitive load task, t(20) = 13.86, p < .001. This indicates that the pattern of relative difficulty between conditions was as expected, with the high-load condition being reliably more challenging.

Comparisons of

Discussion

The aim of this study was to examine the effect of attention on the early pre-movement cortical activity associated with readiness for action, specifically examining the influence of perceptual and cognitive resources on readiness potential amplitudes. Overall, we found that pre-movement neural activity was not influenced by the availability of selective attentional resources in the perceptual load task, whereas it was significantly reduced when cognitive resources were limited under conditions

Acknowledgments

We thank Elysa Whelan for assistance with the perceptual load task. This study was supported by funding from the Australian Research Council to RC (FT0991468).

References (56)

  • M. Erdler et al.

    Supplementary motor area activation preceding voluntary movement is detectable with a whole-scalp magnetoencephalography system

    NeuroImage

    (2000)
  • I. Keller et al.

    Readiness potentials preceding spontaneous motor acts: Voluntary vs. involuntary control

    Electroencephalography and Clinical Neurophysiology

    (1990)
  • J. Kitamura et al.

    A cortical slow potential is larger before an isolated movement of a single finger than simultaneous movement of two fingers

    Electroencephalography and Clinical Neurophysiology

    (1993)
  • H.H. Kornhuber et al.

    Will, volitional action, attention and cerebral potentials in man: Bereitschaftspotential, performance-related potentials, directed attention potential, EEG spectrum changes

  • P.A. Lewis et al.

    Distinct systems for automatic and cognitively controlled time measurement: Evidence from neuroimaging

    Current Opinion in Neurobiology

    (2003)
  • B. Libet et al.

    Readiness-potentials preceding unrestricted ‘spontaneous’ vs. pre-planned voluntary acts

    Electroencephalography and Clinical Neurophysiology

    (1982)
  • F. Macar et al.

    Timing functions of the supplementary motor area: An event-related fMRI study

    Cognitive Brain Research

    (2004)
  • J.S. Mayer et al.

    Common neural substrates for visual working memory and attention

    NeuroImage

    (2007)
  • D.W. McAdam et al.

    Bereitschaftspotential enhancement with increased level of motivation

    Electroencephalography and Clinical Neurophysiology

    (1969)
  • J.J McArdle et al.

    Electrophysiological evidence of functional integration between the language and motor systems in the brain: A study of the speech Bereitschaftspotential

    Clinical Neurophysiology

    (2009)
  • R. Rodriguez-Jimenez et al.

    Differential dorsolateral prefrontal cortex activation during a verbal n-back task according to sensory modality

    Behavioural Brain Research

    (2009)
  • J.B. Rowe et al.

    Attention to action: Specific modulation of corticocortical interactions in humans

    NeuroImage

    (2002)
  • H. Shibasaki et al.

    What is the Bereitschaftspotential?

    Clinical Neurophysiology

    (2006)
  • A.M. Treisman et al.

    A feature-integration theory of attention

    Cognitive Psychology

    (1980)
  • H. Wiese et al.

    Impaired movement-related potentials in acute frontal traumatic brain injury

    Clinical Neurophysiology

    (2004)
  • D. Wildgruber et al.

    Sequential activation of supplementary motor area and primary motor cortex during self-paced finger movement in human evaluated by functional MRI

    Neuroscience Letters

    (1997)
  • D.A. Allport

    Attention and performance

  • A.R. Aron et al.

    Triangulating a cognitive control network using diffusion-weighted magnetic resonance imaging (MRI) and functional MRI

    The Journal of Neuroscience

    (2007)
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