Dissociating effector and movement direction selection during the preparation of manual reaching movements: Evidence from lateralized ERP components

Objective The present study investigated whether lateralized ERP components triggered during covert manual response preparation (ADAN, LDAP) reflect effector selection, the selection of movement direction, or both. Methods Event-related brain potentials were recorded during a response precueing paradigm where visual cues provided either partial (Experiment 1) or full (Experiment 2) information about the response hand and the direction for a subsequent reaching movement. Results ADAN and LDAP components were elicited even when only partial response information was available, demonstrating that they do not require the presence of a fully specified motor program. The ADAN was elicited in a similar fashion regardless of whether effector or movement direction information was provided, suggesting that the underlying mechanisms are equally sensitive to both types of response-related information. In contrast, the LDAP was larger in response to cues providing effector information, but was also reliably present when movement direction was available. Conclusions ADAN and LDAP components reflect preparatory activity within anterior and posterior parts of the parieto-premotor sensorimotor network where different parameters for manual reaching movements are programmed independently. Significance These results support the claim of the premotor theory of attention that shared sensorimotor control mechanisms are involved in attention and motor programming.

[1]  S. Kobayashi,et al.  Electroencephalographic activity associated with shifts of visuospatial attention. , 1994, Brain : a journal of neurology.

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

[3]  Hartmut Leuthold,et al.  Advance movement preparation of eye, foot, and hand: a comparative study using movement-related brain potentials. , 2002, Brain research. Cognitive brain research.

[4]  R. Andersen,et al.  Intention-related activity in the posterior parietal cortex: a review , 2000, Vision Research.

[5]  R. Passingham,et al.  The Attentional Role of the Left Parietal Cortex: The Distinct Lateralization and Localization of Motor Attention in the Human Brain , 2001, Journal of Cognitive Neuroscience.

[6]  I. Jentzsch,et al.  Neural correlates of advance movement preparation: a dipole source analysis approach. , 2001, Brain research. Cognitive brain research.

[7]  Heinrich H Bülthoff,et al.  Effects of pointing direction and direction predictability on event-related lateralizations of the EEG. , 2002, Human movement science.

[8]  Martin Eimer,et al.  Anterior and posterior attentional control systems use different spatial reference frames: ERP evidence from covert tactile-spatial orienting. , 2003, Psychophysiology.

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

[10]  J. Pratt,et al.  Action-centered inhibition: Effects of distractors on movement planning and execution , 1994 .

[11]  U. Castiello,et al.  Effects of left parietal injury on covert orienting of attention , 2002, Journal of neurology, neurosurgery, and psychiatry.

[12]  Paul Cisek,et al.  Neural activity in primary motor and dorsal premotor cortex in reaching tasks with the contralateral versus ipsilateral arm. , 2003, Journal of neurophysiology.

[13]  L. Mulder,et al.  Use of partial stimulus information in response processing. , 1988, Journal of experimental psychology. Human perception and performance.

[14]  Steven W. Keele,et al.  Movement control in skilled motor performance. , 1968 .

[15]  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.

[16]  S. Tipper,et al.  Selective reaching: evidence for action-centered attention. , 1992, Journal of experimental psychology. Human perception and performance.

[17]  M Eimer,et al.  Spatial cueing, sensory gating and selective response preparation: an ERP study on visuo-spatial orienting. , 1993, Electroencephalography and clinical neurophysiology.

[18]  Leslie G. Ungerleider,et al.  Organization of visual inputs to the inferior temporal and posterior parietal cortex in macaques , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[19]  Andrea Brovelli,et al.  EEG dynamics of the frontoparietal network during reaching preparation in humans , 2007, NeuroImage.

[20]  S. Tipper,et al.  Selective reaching: evidence for action-centered attention. , 1992, Journal of experimental psychology. Human perception and performance.

[21]  W. Sommer,et al.  Motor programming of response force and movement direction. , 1998, Psychophysiology.

[22]  a.R.V.,et al.  Clinical neurophysiology , 1961, Neurology.

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

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

[25]  I. Jentzsch,et al.  Beneficial effects of ambiguous precues: parallel motor preparation or reduced premotoric processing time? , 2004, Psychophysiology.

[26]  W. Sommer,et al.  Partial advance information and response preparation: inferences from the lateralized readiness potential. , 1996, Journal of experimental psychology. General.

[27]  A. Sterr,et al.  EEG dipole analysis of motor-priming foreperiod activity reveals separate sources for motor and spatial attention components , 2006, Clinical Neurophysiology.

[28]  M. Goldberg,et al.  Ventral intraparietal area of the macaque: congruent visual and somatic response properties. , 1998, Journal of neurophysiology.

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

[30]  G. Rizzolatti,et al.  The Organization of the Frontal Motor Cortex. , 2000, News in physiological sciences : an international journal of physiology produced jointly by the International Union of Physiological Sciences and the American Physiological Society.

[31]  G. Rizzolatti,et al.  Reorienting attention across the horizontal and vertical meridians: Evidence in favor of a premotor theory of attention , 1987, Neuropsychologia.

[32]  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.

[33]  G. Luppino,et al.  Parietofrontal Circuits for Action and Space Perception in the Macaque Monkey , 2001, NeuroImage.

[34]  D. Rosenbaum.  Human movement initiation: specification of arm, direction, and extent. , 1980, Journal of experimental psychology. General.

[35]  R. Proctor,et al.  Set- and Element-Level Stimulus-Response Compatibility Effects for Different Manual Response Sets. , 1997, Journal of motor behavior.

[36]  Peter Praamstra,et al.  Frontoparietal control of spatial attention and motor intention in human EEG. , 2005, Journal of neurophysiology.

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

[38]  J. Kalaska,et al.  Simultaneous encoding of multiple potential reach directions in dorsal premotor cortex. , 2002, Journal of neurophysiology.

[39]  C. Colby,et al.  Spatial representations for action in parietal cortex. , 1996, Brain research. Cognitive brain research.

[40]  M Eimer,et al.  Stimulus-response compatibility and automatic response activation: evidence from psychophysiological studies. , 1995, Journal of experimental psychology. Human perception and performance.

[41]  R Verleger,et al.  Dimensional overlap between arrows as cueing stimuli and responses?. Evidence from contra-ipsilateral differences in EEG potentials. , 2000, Brain research. Cognitive brain research.

[42]  Otmar Bock,et al.  The mechanisms of movement preparation: a precuing study , 2000, Behavioural Brain Research.

[43]  Peter Praamstra,et al.  Prior information of stimulus location: Effects on ERP measures of visual selection and response selection , 2006, Brain Research.

[44]  J. Miller.  Discrete versus continuous stage models of human information processing: in search of partial output. , 1982, Journal of experimental psychology. Human perception and performance.

[45]  W. Sommer,et al.  Influences of presentation mode and time pressure on the utilisation of advance information in response preparation. , 2002, Acta psychologica.

[46]  Richard A. Andersen,et al.  FMRI evidence for a 'parietal reach region' in the human brain , 2003, Experimental Brain Research.

[47]  Martin Eimer,et al.  Effects of hand posture on preparatory control processes and sensory modulations in tactile-spatial attention , 2004, Clinical Neurophysiology.

[48]  M. Eimer,et al.  Shifts of attention in the early blind: An ERP study of attentional control processes in the absence of visual spatial information , 2006, Neuropsychologia.

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

[50]  Jun Tanji,et al.  Integration of target and body-part information in the premotor cortex when planning action , 2000, Nature.

[51]  Martin Eimer,et al.  Manual response preparation and saccade programming are linked to attention shifts: ERP evidence for covert attentional orienting and spatially specific modulations of visual processing , 2006, Brain Research.

[52]  R. Verleger,et al.  Spatiotemporal overlap between brain activation related to saccade preparation and attentional orienting , 2006, Brain Research.

[53]  Martin H. Fischer,et al.  Attention Allocation During Manual Movement Preparation and Execution , 1997 .

[54]  M. Arbib.  Interaction of multiple representations of space in the brain. , 1991 .

[55]  David Goodman,et al.  Are movements prepared in parts? Not under compatible (naturalized) conditions. , 1980 .

[56]  F. Plum.  Handbook of Physiology. , 1960 .

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

[58]  J. Pratt,et al.  Dissociating visual attention and effector selection in spatial precuing tasks. , 2004, Journal of experimental psychology. Human perception and performance.

[59]  I. Jentzsch,et al.  Distinguishing neural sources of movement preparation and execution An electrophysiological analysis , 2002, Biological Psychology.

[60]  T. G. Reeve,et al.  On the advance preparation of discrete finger responses. , 1984, Journal of experimental psychology. Human perception and performance.

[61]  Jan Theeuwes,et al.  An ERP study of preparatory and inhibitory mechanisms in a cued saccade task , 2006, Brain Research.

[62]  M. Eimer,et al.  Covert manual response preparation triggers attentional modulations of visual but not auditory processing , 2006, Clinical Neurophysiology.

[63]  Martin Eimer,et al.  Covert manual response preparation triggers attentional shifts: ERP evidence for the premotor theory of attention , 2005, Neuropsychologia.

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

[65]  J. Kelso,et al.  Are movements prepared in parts? Not under compatible (naturalized) conditions. , 1980, Journal of experimental psychology. General.

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

[67]  Richard A. Magill,et al.  Memory and control of action , 1983 .

[68]  D. Rosenbaum.  The Movement Precuing Technique: Assumptions, Applications, and Extensions , 1983 .

[69]  M. Desmurget,et al.  An ‘automatic pilot’ for the hand in human posterior parietal cortex: toward reinterpreting optic ataxia , 2000, Nature Neuroscience.

[70]  Anthony R. Dickinson,et al.  Non-spatial, motor-specific activation in posterior parietal cortex , 2002, Nature Neuroscience.