Attentional Cueing at the Saccade Goal, Not at the Target Location, Facilitates Saccades

Presenting a behaviorally irrelevant cue shortly before a target at the same location decreases the latencies of saccades to the target, a phenomenon known as exogenous attention facilitation. It remains unclear whether exogenous attention interacts with early, sensory stages or later, motor planning stages of saccade production. To distinguish between these alternatives, we used a saccadic adaptation paradigm to dissociate the location of the visual target from the saccade goal. Three male and four female human subjects performed both control trials, in which saccades were made to one of two target eccentricities, and adaptation trials, in which the target was shifted from one location to the other during the saccade. This manipulation adapted saccades so that they eventually were directed to the shifted location. In both conditions, a behaviorally irrelevant cue was flashed 66.7 ms before target appearance at a randomly selected one of seven positions that included the two target locations. In control trials, saccade latencies were shortest when the cue was presented at the target location and increased with cue-target distance. In contrast, adapted saccade latencies were shortest when the cue was presented at the adapted saccade goal, and not at the visual target location. The dynamics of adapted saccades were also altered, consistent with prior adaptation studies, except when the cue was flashed at the saccade goal. Overall, the results suggest that attentional cueing facilitates saccade planning rather than visual processing of the target.

[1]  A. Fuchs,et al.  Discharge of monkey nucleus reticularis tegmenti pontis neurons changes during saccade adaptation. , 2005, Journal of neurophysiology.

[2]  A. Opstal,et al.  Transfer of short-term adaptation in human saccadic eye movements , 2004, Experimental Brain Research.

[3]  Richard A. Andersen,et al.  Sensorimotor transformation during eye movements to remembered visual targets , 1991, Vision Research.

[4]  Jillian H. Fecteau,et al.  Neural correlates of the automatic and goal-driven biases in orienting spatial attention. , 2004, Journal of neurophysiology.

[5]  C. J. Erkelens,et al.  Selective adaptation of internally triggered saccades made to visual targets , 2004, Experimental Brain Research.

[6]  H. J. Muller,et al.  Spatial and temporal effects of spatial attention on human saccadic eye movements , 1992, Vision Research.

[7]  J. Findlay,et al.  The Relationship between Eye Movements and Spatial Attention , 1986, The Quarterly journal of experimental psychology. A, Human experimental psychology.

[8]  Jean-Louis Vercher,et al.  Adaptation of voluntary saccades, but not of reactive saccades, transfers to hand pointing movements. , 2007, Journal of neurophysiology.

[9]  Jillian H. Fecteau,et al.  Correlates of Capture of Attention and Inhibition of Return across Stages of Visual Processing , 2005, Journal of Cognitive Neuroscience.

[10]  R. Abrams,et al.  Inhibition of return: effects of attentional cuing on eye movement latencies. , 1994, Journal of experimental psychology. Human perception and performance.

[11]  Dottie M. Clower,et al.  The Inferior Parietal Lobule Is the Target of Output from the Superior Colliculus, Hippocampus, and Cerebellum , 2001, The Journal of Neuroscience.

[12]  J. Findlay,et al.  Express saccades: is there a separate population in humans? , 2004, Experimental Brain Research.

[13]  J. V. Van Gisbergen,et al.  Short-term adaptation of electrically induced saccades in monkey superior colliculus. , 1996, Journal of neurophysiology.

[14]  P. Gelder,et al.  Peak velocities of visually and nonvisually guided saccades in smooth-pursuit and saccadic tasks , 1997, Experimental Brain Research.

[15]  A. Fuchs,et al.  Saccadic gain modification: visual error drives motor adaptation. , 1998, Journal of neurophysiology.

[16]  David L. Sparks,et al.  Systematic errors for saccades to remembered targets: Evidence for a dissociation between saccade metrics and activity in the superior colliculus , 1994, Vision Research.

[17]  J E Albano,et al.  Rapid adaptation of saccadic amplitude in humans and monkeys. , 1989, Investigative ophthalmology & visual science.

[18]  M. Posner,et al.  Neural systems control of spatial orienting. , 1982, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[19]  Christopher T. Noto,et al.  Characteristics of simian adaptation fields produced by behavioral changes in saccade size and direction. , 1999, Journal of neurophysiology.

[20]  J. V. Gisbergen,et al.  A parametric analysis of human saccades in different experimental paradigms , 1987, Vision Research.

[21]  A. Fuchs,et al.  The brainstem burst generator for saccadic eye movements , 2002, Experimental Brain Research.

[22]  D H Brainard,et al.  The Psychophysics Toolbox. , 1997, Spatial vision.

[23]  M. Goldberg,et al.  Effect of short-term saccadic adaptation on saccades evoked by electrical stimulation in the primate superior colliculus. , 2002, Journal of neurophysiology.

[24]  A. Fuchs,et al.  Transfer of gain changes from targeting to other types of saccade in the monkey: constraints on possible sites of saccadic gain adaptation. , 1996, Journal of neurophysiology.

[25]  Denis Pélisson,et al.  Behavioral evidence of separate adaptation mechanisms controlling saccade amplitude lengthening and shortening. , 2009, Journal of neurophysiology.

[26]  A. Fuchs,et al.  Characteristics of saccadic gain adaptation in rhesus macaques. , 1997, Journal of neurophysiology.

[27]  Albert F Fuchs,et al.  Activity changes in monkey superior colliculus during saccade adaptation. , 2007, Journal of neurophysiology.

[28]  F R Robinson,et al.  Visual error is the stimulus for saccade gain adaptation. , 2001, Brain research. Cognitive brain research.

[29]  Heiner Deubel,et al.  Adaptive Control of Saccade Metrics , 1991 .

[30]  M E Goldberg,et al.  Dependence of saccade-related activity in the primate superior colliculus on visual target presence. , 2001, Journal of neurophysiology.

[31]  Bruce Bridgeman,et al.  Failure to detect displacement of the visual world during saccadic eye movements , 1975, Vision Research.

[32]  A. Opstal,et al.  Monkey Superior Colliculus Activity During Short-Term Saccadic Adaptation , 1997, Brain Research Bulletin.

[33]  R. W. Kentridge,et al.  Independent contributions of the orienting of attention, fixation offset and bilateral stimulation on human saccadic latencies , 2004, Experimental Brain Research.

[34]  Eileen Kowler,et al.  The control of saccadic adaptation: implications for the scanning of natural visual scenes , 2000, Vision Research.

[35]  Heiner Deubel,et al.  Rapid gain adaptation affects the dynamics of saccadic eye movements in humans , 1995, Vision Research.

[36]  Jillian H. Fecteau,et al.  Using auditory and visual stimuli to investigate the behavioral and neuronal consequences of reflexive covert orienting. , 2004, Journal of neurophysiology.

[37]  M. Schlag-Rey,et al.  Primate antisaccades. I. Behavioral characteristics. , 1998, Journal of neurophysiology.

[38]  E Kowler,et al.  Illusory shifts in visual direction accompany adaptation of saccadic eye movements , 1999, Nature.

[39]  J. Vercher,et al.  Mechanisms of short-term saccadic adaptation. , 1989, Journal of experimental psychology. Human perception and performance.

[40]  P. May The mammalian superior colliculus: laminar structure and connections. , 2006, Progress in brain research.

[41]  S. C. Mclaughlin Parametric adjustment in saccadic eye movements , 1967 .

[42]  A. Fuchs,et al.  The characteristics and neuronal substrate of saccadic eye movement plasticity , 2004, Progress in Neurobiology.

[43]  D G Pelli,et al.  The VideoToolbox software for visual psychophysics: transforming numbers into movies. , 1997, Spatial vision.

[44]  Kitty Z. Xu,et al.  Inhibition of voluntary saccadic eye movement commands by abrupt visual onsets. , 2009, Journal of neurophysiology.

[45]  J D Holtzman,et al.  Components of visual attention. Alterations in response pattern to visual stimuli following parietal lobe infarction. , 1986, Brain : a journal of neurology.

[46]  Robert J Snowden,et al.  Visual Attention to Color: Parvocellular Guidance of Attentional Resources? , 2002, Psychological science.

[47]  H Deubel,et al.  Adaptive gain control of saccadic eye movements. , 1986, Human neurobiology.

[48]  A. C. Smit,et al.  A short-latency transition in saccade dynamics during square-wave tracking and its significance for the differentiation of visually-guided and predictive saccades , 2004, Experimental Brain Research.

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

[50]  D. Sparks,et al.  Site and parameters of microstimulation: evidence for independent effects on the properties of saccades evoked from the primate superior colliculus. , 1996, Journal of neurophysiology.

[51]  J. Rovamo,et al.  An estimation and application of the human cortical magnification factor , 2004, Experimental Brain Research.

[52]  S. Yantis,et al.  Visual attention: control, representation, and time course. , 1997, Annual review of psychology.

[53]  Jay A. Edelman,et al.  Antisaccade velocity, but not latency, results from a lack of saccade visual guidance , 2006, Vision Research.

[54]  Scott T. Grafton,et al.  Genetic dissection of Alzheimer's disease and related dementias: amyloid and its relationship to tau , 1998, Nature Neuroscience.

[55]  F. Lui,et al.  Projections from visual areas of the cerebral cortex to pretectal nuclear complex, terminal accessory optic nuclei, and superior colliculus in macaque monkey , 1995, The Journal of comparative neurology.

[56]  Thérèse Collins,et al.  Saccade dynamics before, during, and after saccadic adaptation in humans. , 2008, Investigative ophthalmology & visual science.