Interactions between endogenous and exogenous attention on cortical visual processing

Sensory processing is affected by both endogenous and exogenous mechanisms of attention, although how these mechanisms interact in the brain has remained unclear. In the present study, we recorded event-related potentials (ERPs) to investigate how multiple stages of information processing in the brain are affected when endogenous and exogenous mechanisms are concurrently engaged. We found that the earliest stage of cortical visual processing, the striate-cortex-generated C1, was immune to attentional modulation, even when endogenous and exogenous attention converged on a common location. The earliest stage of processing to be affected in this experiment was the late phase of the extrastriate-cortex-generated P1 component, which was dominated by exogenous attention. Processing at this stage was enhanced by exogenous attention, regardless of where endogenous attention had been oriented. Endogenous attention, however, dominated a later, higher-order stage of processing indexed by an enhancement of the P300 that was unaffected by exogenous attention. Critically, between these early and late stages, an interaction was found wherein endogenous and exogenous attention produced distinct, and overlapping, effects on information processing. At the same time that exogenous attention was producing an extended enhancement of the late-P1, endogenous attention was enhancing the occipital-parietal N1 component. These results provide neurophysiological support for theories suggesting that endogenous and exogenous mechanisms represent two attention systems that can affect information processing in the brain in distinct ways. Furthermore, these data provide new evidence regarding the precise stages of neural processing that are, and are not, affected when endogenous and exogenous attentions interact.

[1]  Anthony J. Ries,et al.  Automatic Versus Contingent Mechanisms of Sensory-Driven Neural Biasing and Reflexive Attention , 2005, Journal of Cognitive Neuroscience.

[2]  S. Hillyard,et al.  Delayed Striate Cortical Activation during Spatial Attention , 2002, Neuron.

[3]  P. Rabbitt,et al.  Reflexive and voluntary orienting of visual attention: time course of activation and resistance to interruption , 1989 .

[4]  A. Nobre,et al.  The Large-Scale Neural Network for Spatial Attention Displays Multifunctional Overlap But Differential Asymmetry , 1999, NeuroImage.

[5]  G. Mangun,et al.  Covariations in ERP and PET measures of spatial selective attention in human extrastriate visual cortex , 1997, Human brain mapping.

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

[7]  Stephen M. Rao,et al.  Neural Basis of Endogenous and Exogenous Spatial Orienting: A Functional MRI Study , 1999, Journal of Cognitive Neuroscience.

[8]  M. Goldberg,et al.  Neuronal Activity in the Lateral Intraparietal Area and Spatial Attention , 2003, Science.

[9]  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.

[10]  G R Mangun,et al.  Combined expectancies: event-related potentials reveal the early benefits of spatial attention that are obscured by reaction time measures. , 2001, Journal of experimental psychology. Human perception and performance.

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

[12]  G R Mangun,et al.  Attention and spatial selection: Electrophysiological evidence for modulation by perceptual load , 2000, Perception & psychophysics.

[13]  Alan Kingstone,et al.  Abrupt onsets and gaze direction cues trigger independent reflexive attentional effects , 2003, Cognition.

[14]  J. Theeuwes,et al.  On the time course of top-down and bottom-up control of visual attention , 2000 .

[15]  S. Hillyard,et al.  Visual evoked potentials and selective attention to points in space , 1977 .

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

[17]  J. Hopfinger,et al.  Appearing and disappearing stimuli trigger a reflexive modulation of visual cortical activity. , 2005, Brain research. Cognitive brain research.

[18]  R. Desimone,et al.  Neural mechanisms of selective visual attention. , 1995, Annual review of neuroscience.

[19]  L. M. Ward,et al.  Inhibition of Return From Stimulus to Response , 2004, Psychological science.

[20]  J. C. Johnston,et al.  Involuntary covert orienting is contingent on attentional control settings. , 1992, Journal of experimental psychology. Human perception and performance.

[21]  George R. Mangun,et al.  Reflexive Attention Modulates Processing of Visual Stimuli in Human Extrastriate Cortex , 1998, Psychological science.

[22]  Shihui Han,et al.  Shifts of spatial attention in perceived 3-D space , 2005, The Quarterly journal of experimental psychology. A, Human experimental psychology.

[23]  R. Barry,et al.  EOG correction: which regression should we use? , 2000, Psychophysiology.

[24]  S. Hillyard,et al.  Spatial Selective Attention Affects Early Extrastriate But Not Striate Components of the Visual Evoked Potential , 1996, Journal of Cognitive Neuroscience.

[25]  Shimin Fu,et al.  The attentional effects of peripheral cueing as revealed by two event-related potential studies , 2001, Clinical Neurophysiology.

[26]  R. Klein,et al.  Perceptual-motor expectancies interact with covert visual orienting under conditions of endogenous but not exogenous control. , 1994, Canadian journal of experimental psychology = Revue canadienne de psychologie experimentale.

[27]  M. Corbetta,et al.  A PET study of visuospatial attention , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[28]  M. Posner,et al.  Components of visual orienting , 1984 .

[29]  Christopher Kennard,et al.  Differential cortical activation during voluntary and reflexive saccades in man , 2003, NeuroImage.

[30]  S. Luck,et al.  Spatio‐temporal dynamics of attention to color: Evidence from human electrophysiology , 1998, Human brain mapping.

[31]  E Donchin,et al.  The time constant in P300 recording. , 1979, Psychophysiology.

[32]  Richard B Buxton,et al.  Putting spatial attention on the map: timing and localization of stimulus selection processes in striate and extrastriate visual areas , 2001, Vision Research.

[33]  R. Klein,et al.  Is Posner's "beam" the same as Treisman's "glue"?: On the relation between visual orienting and feature integration theory. , 1987, Journal of experimental psychology. Human perception and performance.

[34]  Raja Parasuraman,et al.  Event-related potentials reveal dissociable mechanisms for orienting and focusing visuospatial attention. , 2005, Brain research. Cognitive brain research.

[35]  M. Cheal,et al.  Central and Peripheral Precuing of Forced-Choice Discrimination , 1991, The Quarterly journal of experimental psychology. A, Human experimental psychology.

[36]  M. Russell Harter,et al.  Effects of attention and arousal on visually evoked cortical potentials and reaction time in man , 1969 .

[37]  Alan Kingstone,et al.  Attentional effects of counterpredictive gaze and arrow cues. , 2004, Journal of experimental psychology. Human perception and performance.

[38]  S. Hillyard,et al.  Involvement of striate and extrastriate visual cortical areas in spatial attention , 1999, Nature Neuroscience.

[39]  Richard S. J. Frackowiak,et al.  Functional localization of the system for visuospatial attention using positron emission tomography. , 1997, Brain : a journal of neurology.

[40]  S. Hillyard,et al.  Modulations of sensory-evoked brain potentials indicate changes in perceptual processing during visual-spatial priming. , 1991, Journal of experimental psychology. Human perception and performance.

[41]  Steven J. Luck,et al.  Multiple mechanisms of visual-spatial attention: recent evidence from human electrophysiology , 1995, Behavioural Brain Research.

[42]  J. Jonides Voluntary versus automatic control over the mind's eye's movement , 1981 .

[43]  Lawrence M. Ward,et al.  An event-related brain potential study of inhibition of return , 1999, Perception & psychophysics.

[44]  Jan Theeuwes,et al.  Endogenous and exogenous attention shifts are mediated by the same large-scale neural network , 2004, NeuroImage.

[45]  K. Briand,et al.  Feature integration and spatial attention : More evidence of a dissociation between endogenous and exogenous orienting , 1998 .

[46]  G. Mangun,et al.  Perceptual Load and Visuocortical Processing: Event-Related Potentials Reveal Sensory-Level Selection , 2001, Psychological science.

[47]  S. Yantis,et al.  Abrupt visual onsets and selective attention: voluntary versus automatic allocation. , 1990, Journal of experimental psychology. Human perception and performance.

[48]  S. Hillyard,et al.  Cortical sources of the early components of the visual evoked potential , 2002, Human brain mapping.

[49]  M. Gazzaniga,et al.  Combined spatial and temporal imaging of brain activity during visual selective attention in humans , 1994, Nature.

[50]  Andrew R. Mayer,et al.  Neural networks underlying endogenous and exogenous visual–spatial orienting , 2004, NeuroImage.

[51]  S. Luck,et al.  Are the Same Attentional Mechanisms Used to Detect Visual Search Targets Defined by Color, Orientation, and Motion? , 1997, Journal of Cognitive Neuroscience.

[52]  G R Mangun,et al.  Tracking the influence of reflexive attention on sensory and cognitive processing , 2001, Cognitive, affective & behavioral neuroscience.

[53]  S J Luck,et al.  Spatial filtering during visual search: evidence from human electrophysiology. , 1994, Journal of experimental psychology. Human perception and performance.

[54]  M. Woldorff,et al.  Distortion of ERP averages due to overlap from temporally adjacent ERPs: analysis and correction. , 2007, Psychophysiology.