Early event-related potentials indicate context-specific target processing for eye and hand motor systems

Concurrent eye and hand movements toward a common visual target require different motor programs based on identical visual input. We used event-related brain potentials (ERP) to determine if and when the processing of the visual target differs for the two motor systems. The N2, an index for target evaluation, was more negative for the target of a hand than of an eye movement in two experiments. A possible interpretation for this finding is different visual target processing. Targets for hand movements require a different weighting of visual information, for example concerning features such as surface structure which are important for hand but not for eye movements. In experiment 2, the early C1-component, which had an average maximum at 67 ms following target onset, was significantly more negative when subjects pointed at the stimuli. Traditionally, the C1 has been regarded as a sensory component, but recent studies have linked it to higher order processing, such as attention and expectations. Thus, the present data indicate that target processing for eye or hand movements is already context-specific during early visual information processing. We suggest that differences in a target's relevance for upcoming movements modify target processing as well as sensory expectations.

[1]  P. Zipp,et al.  Recommendations for the standardization of lead positions in surface electromyography , 1982, European Journal of Applied Physiology and Occupational Physiology.

[2]  H. Bekkering,et al.  Transfer of saccadic adaptation to the manual motor system , 1995 .

[3]  K. Suemitsu,et al.  Object recognition learning differentiates the representations of objects at the ERP component N1 , 2007, Clinical Neurophysiology.

[4]  M. Goodale,et al.  Visual control of reaching movements without vision of the limb , 2004, Experimental Brain Research.

[5]  Elena Gherri,et al.  The orienting of attention during eye and hand movements: ERP evidence for similar frame of reference but different spatially specific modulations of tactile processing , 2012, Biological Psychology.

[6]  F A GIBBS,et al.  A balanced non-cephalic reference electrode. , 1951, Electroencephalography and clinical neurophysiology.

[7]  B. Kopp,et al.  N2, P3 and the lateralized readiness potential in a nogo task involving selective response priming. , 1996, Electroencephalography and clinical neurophysiology.

[8]  Jonathan D. Cohen,et al.  Stimulus modality, perceptual overlap, and the go/no-go N2. , 2004, Psychophysiology.

[9]  S. Hillyard,et al.  Identification of early visual evoked potential generators by retinotopic and topographic analyses , 1994 .

[10]  W Pieter Medendorp,et al.  Behavioral reference frames for planning human reaching movements. , 2006, Journal of neurophysiology.

[11]  E. Vogel,et al.  The visual N1 component as an index of a discrimination process. , 2000, Psychophysiology.

[12]  Fernando Cadaveira,et al.  N2pc and attentional capture by colour and orientation-singletons in pure and mixed visual search tasks. , 2009, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[13]  G. Pourtois,et al.  Attentional load modifies early activity in human primary visual cortex , 2009, Human brain mapping.

[14]  Raja Parasuraman,et al.  Attentional load is not a critical factor for eliciting C1 attentional effect – A reply to Rauss, Pourtois, Vuilleumier, and Schwartz , 2012, Biological Psychology.

[15]  R. C. Oldfield.  The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[16]  Arnaud Delorme,et al.  EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis , 2004, Journal of Neuroscience Methods.

[17]  H. Bauer,et al.  Operant conditioning of brain steady potential shifts in man , 1979, Biofeedback and self-regulation.

[18]  Salil H. Patel,et al.  Characterization of N200 and P300: Selected Studies of the Event-Related Potential , 2005, International journal of medical sciences.

[19]  M. Jeannerod,et al.  Selective perturbation of visual input during prehension movements , 1991, Experimental Brain Research.

[20]  Cheryl L. Dickter,et al.  Strategic control and medial frontal negativity: beyond errors and response conflict. , 2005, Psychophysiology.

[21]  L. Carlton.  Processing visual feedback information for movement control. , 1981, Journal of experimental psychology. Human perception and performance.

[22]  H. Jasper,et al.  The ten-twenty electrode system of the International Federation. The International Federation of Clinical Neurophysiology. , 1999, Electroencephalography and clinical neurophysiology. Supplement.

[23]  W Pieter Medendorp,et al.  Three-dimensional transformations for goal-directed action. , 2011, Annual review of neuroscience.

[24]  Marzia Del Zotto,et al.  Electrical neuroimaging evidence that spatial frequency-based selective attention affects V1 activity as early as 40-60 ms in humans , 2010, BMC Neuroscience.

[25]  P. Donkelaar,et al.  Saccade amplitude influences pointing movement kinematics. , 1998 .

[26]  J. Douglas Crawford,et al.  Specialization of reach function in human posterior parietal cortex , 2012, Experimental Brain Research.

[27]  John J. Foxe,et al.  Spatial attention modulates initial afferent activity in human primary visual cortex. , 2008, Cerebral cortex.

[28]  M. Corbetta,et al.  Extrastriate body area in human occipital cortex responds to the performance of motor actions , 2004, Nature Neuroscience.

[29]  Uta Sailer,et al.  Implications of distracter effects for the organization of eye movements, hand movements, and perception. , 2002, Progress in brain research.

[30]  Claus Lamm,et al.  Individual differences in brain activity during visuo-spatial processing assessed by slow cortical potentials and LORETA. , 2005, Brain research. Cognitive brain research.

[31]  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.

[32]  S. Kosslyn,et al.  Neural foundations of imagery , 2001, Nature Reviews Neuroscience.

[33]  Uta Sailer,et al.  Global effect of a nearby distractor on targeting eye and hand movements. , 2002, Journal of experimental psychology. Human perception and performance.

[34]  S. Luck.  An Introduction to the Event-Related Potential Technique , 2005 .

[35]  István Czigler,et al.  Age-related effects of novel visual stimuli in a letter-matching task: an event-related potential study , 2005, Biological Psychology.

[36]  Antigona Martínez,et al.  Source analysis of event-related cortical activity during visuo-spatial attention. , 2003, Cerebral cortex.

[37]  G. Pourtois,et al.  Top-down effects on early visual processing in humans: A predictive coding framework , 2011, Neuroscience & Biobehavioral Reviews.

[38]  David C Knill,et al.  Decoupling eye and hand movement control: visual short-term memory influences reach planning more than saccade planning. , 2012, Journal of vision.

[39]  D. Tucker,et al.  Frontal evaluation and posterior representation in target detection. , 2001, Brain research. Cognitive brain research.

[40]  Victor A. F. Lamme,et al.  Neural Mechanisms of Visual Awareness: A Linking Proposition , 2000 .

[41]  Marc Hassenzahl,et al.  Haptic texture affects the kinematics of pointing movements, but not of eye movements , 2003, Neuroreport.