Covert manual response preparation triggers attentional shifts: ERP evidence for the premotor theory of attention

The premotor theory of attention claims that the preparation of goal-directed action and shifts of attention are closely linked, because they are controlled by shared sensorymotor mechanisms. Until now, support for this theory has come primarily from studies demonstrating links between saccade programming and attention shifts. The present event-related brain potential (ERP) study demonstrated that attentional orienting processes are also elicited during the covert preparation of unimanual responses. ERPs were recorded in the interval between a visual response-hand selection cue and a subsequent visual Go/Nogo signal when participants prepared to lift their left or right index finger. Lateralised ERP components elicited during response preparation were very similar to components previously observed during instructed endogenous attention shifts, indicating that analogous attentional orienting processes are activated in both cases. Somatosensory ERP components (P90, N140) were enhanced when task-irrelevant tactile probes were delivered during response preparation to the hand involved in an anticipated response, even when probes were presented well in advance of response execution. These results suggest that attentional shifts are triggered during unimanual response preparation, as predicted by the premotor theory. This link between manual response programming and attention is consistent with the hypothesis that common mechanisms are involved in the control of attention and action.

[1]  C. E. Chapman,et al.  Time course and magnitude of movement-related gating of tactile detection in humans. I. Importance of stimulus location. , 1998, Journal of neurophysiology.

[2]  J. Hoffman,et al.  The role of visual attention in saccadic eye movements , 1995, Perception & psychophysics.

[3]  Jon Driver,et al.  Shifts of attention in light and in darkness: an ERP study of supramodal attentional control and crossmodal links in spatial attention. , 2003, Brain research. Cognitive brain research.

[4]  Martin Eimer,et al.  Crossmodal links in spatial attention are mediated by supramodal control processes: evidence from event-related potentials. , 2002, Psychophysiology.

[5]  Beverly C. Butler,et al.  Gradients of detection in neglect: comparison of peripersonal and extrapersonal space , 2004, Neuropsychologia.

[6]  Martin Eimer,et al.  The Lateralized Readiness Potential , 2003 .

[7]  C. Gross,et al.  Coding of visual space by premotor neurons. , 1994, Science.

[8]  M. Posner,et al.  The attention system of the human brain. , 1990, Annual review of neuroscience.

[9]  J C Rothwell,et al.  Pre-movement gating of short-latency somatosensory evoked potentials. , 1999, Neuroreport.

[10]  F. Mauguière,et al.  Somatosensory responses during selective spatial attention: The N120‐to‐N140 trasition , 1995 .

[11]  David E. Irwin Robert D. Gordon Eye Movements, Attention and Trans-saccadic Memory , 1998 .

[12]  Carla M. Bosco,et al.  Event-related brain potentials as indices of information extraction and response priming. , 1990, Electroencephalography and clinical neurophysiology.

[13]  F. Rösler,et al.  Crossmodal and intermodal attention modulate event-related brain potentials to tactile and auditory stimuli , 2002, Experimental Brain Research.

[14]  D. Robinson,et al.  Shared neural control of attentional shifts and eye movements , 1996, Nature.

[15]  J Driver,et al.  An event-related brain potential study of cross-modal links in spatial attention between vision and touch. , 2000, Psychophysiology.

[16]  G. Rizzolatti,et al.  Space and selective attention , 1994 .

[17]  G. R Mangun,et al.  Shifting visual attention in space: an electrophysiological analysis using high spatial resolution mapping , 2000, Clinical Neurophysiology.

[18]  R. M. Siegel,et al.  Neurons of area 7 activated by both visual stimuli and oculomotor behavior , 2004, Experimental Brain Research.

[19]  R. Andersen,et al.  Coding of intention in the posterior parietal cortex , 1997, Nature.

[20]  H. Deubel,et al.  Saccade target selection and object recognition: Evidence for a common attentional mechanism , 1996, Vision Research.

[21]  A. Nobre,et al.  The dynamics of shifting visuospatial attention revealed by event-related potentials , 2000, Neuropsychologia.

[22]  Pre-movement gating of shortlatency somatosensory evoked potentialsに関する研究 : 短潜時体性感覚誘発電位の運動準備状態での変化 , 2000 .

[23]  R. Andersen,et al.  Intentional maps in posterior parietal cortex. , 2002, Annual review of neuroscience.

[24]  G. Rizzolatti,et al.  Spatial attention and eye movements , 2004, Experimental Brain Research.

[25]  Martin Eimer,et al.  The lateralized readiness potential as an on-line measure of central response activation processes , 1998 .

[26]  J. Driver,et al.  Crossmodal links in endogenous and exogenous spatial attention: evidence from event-related brain potential studies , 2001, Neuroscience & Biobehavioral Reviews.

[27]  M. Corbetta,et al.  A Common Network of Functional Areas for Attention and Eye Movements , 1998, Neuron.

[28]  F. Mauguière,et al.  Timing and spatial distribution of somatosensory responses recorded in the upper bank of the sylvian fissure (SII area) in humans. , 1999, Cerebral cortex.

[29]  M. Goodale,et al.  Separate visual pathways for perception and action , 1992, Trends in Neurosciences.

[30]  Steven L. Miller,et al.  Neural Processes Involved in Directing Attention , 1989, Journal of Cognitive Neuroscience.

[31]  J. Marshall,et al.  Left neglect for near but not far space in man , 1991, Nature.

[32]  Martin Eimer,et al.  Early posterior ERP components do not reflect the control of attentional shifts toward expected peripheral events. , 2003, Psychophysiology.

[33]  Martin Eimer,et al.  The spatial distribution of attentional selectivity in touch: evidence from somatosensory ERP components , 2003, Clinical Neurophysiology.

[34]  E. Donchin,et al.  Probability effects on stimulus evaluation and response processes. , 1992, Journal of experimental psychology. Human perception and performance.

[35]  M. Eimer,et al.  Modulations of early somatosensory ERP components by transient and sustained spatial attention , 2003, Experimental Brain Research.

[36]  Claudio Babiloni,et al.  “Gating” of human short-latency somatosensory evoked cortical responses during execution of movement. A high resolution electroencephalography study , 1999, Brain Research.

[37]  F. Mauguière,et al.  Intracortical recordings of early pain-related CO2-laser evoked potentials in the human second somatosensory (SII) area , 1999, Clinical Neurophysiology.

[38]  P M Rossini,et al.  Somatosensory evoked potentials during the ideation and execution of individual finger movements , 1996, Muscle & nerve.

[39]  Martin Eimer,et al.  Temporal dynamics of lateralized ERP components elicited during endogenous attentional shifts to relevant tactile events. , 2002, Psychophysiology.

[40]  R Verleger,et al.  Lateralised cortical activity due to preparation of saccades and finger movements: a comparative study. , 1997, Electroencephalography and clinical neurophysiology.

[41]  J. Driver,et al.  Does auditory attention shift in the direction of an upcoming saccade? , 1999, Neuropsychologia.

[42]  Jon Driver,et al.  Cross-Modal Interactions between Audition, Touch, and Vision in Endogenous Spatial Attention: ERP Evidence on Preparatory States and Sensory Modulations , 2002, Journal of Cognitive Neuroscience.

[43]  A. Berti,et al.  When Far Becomes Near: Remapping of Space by Tool Use , 2000, Journal of Cognitive Neuroscience.

[44]  P. Michie,et al.  The effects of spatial selective attention on the somatosensory event-related potential. , 1987, Psychophysiology.

[45]  Chris Rorden,et al.  Enhanced Tactile Performance at the Destination of an Upcoming Saccade , 2002, Current Biology.

[46]  T Landis,et al.  Near and far visual space in unilateral neglect , 1998, Annals of neurology.

[47]  Rolf Verleger,et al.  Lateralized EEG components with direction information for the preparation of saccades versus finger movements , 2000, Experimental Brain Research.

[48]  L. Cohen,et al.  ‘Gating’ of somatosensory evoked potentials begins before the onset of voluntary movement in man , 1985, Brain Research.