Neural correlates of spatial orienting in the human superior colliculus.

A natural visual scene contains more information than the visual system has the capacity to simultaneously process, requiring specific items to be selected for detailed analysis at the expense of others. Such selection and inhibition are fundamental in guiding search behavior, but the neural basis of these mechanisms remains unclear. Abruptly appearing visual items can automatically capture attention, but once attention has been directed away from the salient event, return to that same location is slowed. In non-human primates, signals associated with attentional capture (AC) and subsequent inhibition of return (IOR) have been recorded from the superior colliculus (SC)--a structure known to play a pivotal role in reflexive spatial orienting. Here, we sought to establish whether similar signals could be recorded from the human SC, as well as early retinotopic cortical visual areas, where signals associated with AC and IOR have yet to be investigated with respect to oculomotor responses. Using an optimized oculomotor paradigm together with high-field, high-spatial resolution functional magnetic resonance imaging and high-speed eye tracking, we demonstrate that BOLD signal changes recorded from the human SC correlate strongly with our saccadic measures of AC and IOR. A qualitatively similar pattern of responses was found for V1, but only the inhibitory response associated with IOR persisted through V2 and V3. Although the SC plays a role in mediating these automatic attentional biasing signals, the source of these signals is likely to lie in higher cortical areas.

[1]  J. Lupiáñez,et al.  Does IOR occur in discrimination tasks? Yes, it does, but later , 1997, Perception & psychophysics.

[2]  R. Lund Anatomic studies on the superior colliculus. , 1972, Investigative ophthalmology.

[3]  R. Abrams,et al.  The gap effect and inhibition of return: interactive effects on eye movement latencies , 2004, Experimental Brain Research.

[4]  Andrew T. Smith,et al.  Functional imaging of the human superior colliculus: An optimised approach , 2009, NeuroImage.

[5]  M E Wilson,et al.  Retino-tectal and cortico-tectal projections in Macaca mulatta. , 1970, Brain research.

[6]  Mark S. Cohen,et al.  Spatiotopic Organization in Human Superior Colliculus Observed with fMRI , 2000, NeuroImage.

[7]  R. Klein,et al.  Inhibition of Return is a Foraging Facilitator in Visual Search , 1999 .

[8]  Katherine M. Armstrong,et al.  Visual and oculomotor selection: links, causes and implications for spatial attention , 2006, Trends in Cognitive Sciences.

[9]  J. Pratt,et al.  Inhibition of return is composed of attentional and oculomotor processes , 1999, Perception & psychophysics.

[10]  A M Graybiel,et al.  The differential projection of two cytoarchitectonic subregions of the inferior parietal lobule of macaque upon the deep layers of the superior colliculus , 1985, The Journal of comparative neurology.

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

[12]  M. Posner,et al.  Inhibition of return : Neural basis and function , 1985 .

[13]  R. Klein,et al.  Two mechanisms underlying inhibition of return , 2010, Experimental Brain Research.

[14]  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.

[15]  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.

[16]  Karl J. Friston,et al.  Functional Anatomy of Visual Search: Regional Segregations within the Frontal Eye Fields and Effective Connectivity of the Superior Colliculus , 2002, NeuroImage.

[17]  Avishai Henik,et al.  Inhibition of return in spatial attention: direct evidence for collicular generation , 1999, Nature Neuroscience.

[18]  R. Wurtz,et al.  Monkey posterior parietal cortex neurons antidromically activated from superior colliculus. , 1997, Journal of neurophysiology.

[19]  R. Rafal,et al.  Contributions of the human pulvinar to linking vision and action , 2004, Cognitive, affective & behavioral neuroscience.

[20]  A. Song,et al.  The Saccadic Re-Centering Bias is Associated with Activity Changes in the Human Superior Colliculus , 2010, Front. Hum. Neurosci..

[21]  J. Theeuwes Top-down and bottom-up control of visual selection. , 2010, Acta psychologica.

[22]  Raymond Klein,et al.  Inhibitory tagging system facilitates visual search , 1988, Nature.

[23]  C. Kennard,et al.  Distinct Cortical and Collicular Mechanisms of Inhibition of Return Revealed with S Cone Stimuli , 2004, Current Biology.

[24]  J. Theeuwes,et al.  Oculomotor capture and Inhibition of Return: Evidence for an oculomotor suppression account of IOR , 2002, Psychological research.

[25]  N. P. Bichot,et al.  Priming in Macaque Frontal Cortex during Popout Visual Search: Feature-Based Facilitation and Location-Based Inhibition of Return , 2002, The Journal of Neuroscience.

[26]  Geraint Rees,et al.  Visual FMRI responses in human superior colliculus show a temporal-nasal asymmetry that is absent in lateral geniculate and visual cortex. , 2007, Journal of neurophysiology.

[27]  Andreas Kleinschmidt,et al.  Temporal Dynamics of the Attentional Spotlight: Neuronal Correlates of Attentional Capture and Inhibition of Return in Early Visual Cortex , 2007, Journal of Cognitive Neuroscience.

[28]  Jillian H. Fecteau,et al.  Salience, relevance, and firing: a priority map for target selection , 2006, Trends in Cognitive Sciences.

[29]  Laurent Petit,et al.  Neural basis of visually guided head movements studied with fMRI. , 2003, Journal of neurophysiology.

[30]  Jan Theeuwes,et al.  Unconscious cueing effects in saccadic eye movements – Facilitation and inhibition in temporal and nasal hemifield , 2010, Vision Research.

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

[32]  Activation of superior colliculi in humans during visual exploration , 2007, BMC Neuroscience.

[33]  M. Rothbart,et al.  Development of orienting to locations and objects in human infants. , 1994, Canadian journal of experimental psychology = Revue canadienne de psychologie experimentale.

[34]  W. Fries Cortical projections to the superior colliculus in the macaque monkey: A retrograde study using horseradish peroxidase , 1984, The Journal of comparative neurology.

[35]  J W Belliveau,et al.  Borders of multiple visual areas in humans revealed by functional magnetic resonance imaging. , 1995, Science.

[36]  M. Carrasco,et al.  Transient Attention Enhances Perceptual Performance and fMRI Response in Human Visual Cortex , 2005, Neuron.

[37]  R. Rafal,et al.  Components of reflexive visual orienting to moving objects , 1999, Perception & psychophysics.

[38]  Stephen D. Mayhew,et al.  Determination of the human brainstem respiratory control network and its cortical connections in vivo using functional and structural imaging , 2009, NeuroImage.

[39]  Sabine Kastner,et al.  Visual responses of the human superior colliculus: a high-resolution functional magnetic resonance imaging study. , 2005, Journal of neurophysiology.

[40]  P. Calabresi,et al.  Saccade preparation inhibits reorienting to recently attended locations. , 1989, Journal of experimental psychology. Human perception and performance.

[41]  Karl J. Friston,et al.  Stochastic Designs in Event-Related fMRI , 1999, NeuroImage.

[42]  Robert D. Rafal,et al.  Inhibitory Tagging of Locations in the Blind Field of Hemianopic Patients , 1997, Consciousness and Cognition.

[43]  G H Glover,et al.  Image‐based method for retrospective correction of physiological motion effects in fMRI: RETROICOR , 2000, Magnetic resonance in medicine.

[44]  D P Munoz,et al.  On your mark, get set: brainstem circuitry underlying saccadic initiation. , 2000, Canadian journal of physiology and pharmacology.

[45]  S. Pollmann,et al.  Covert Reorienting and Inhibition of Return: An Event-Related fMRI Study , 2002, Journal of Cognitive Neuroscience.

[46]  Peter A. Bandettini,et al.  Separating respiratory-variation-related fluctuations from neuronal-activity-related fluctuations in fMRI , 2006, NeuroImage.

[47]  Petroc Sumner,et al.  Human intraparietal sulcus (IPS) and competition between exogenous and endogenous saccade plans , 2008, NeuroImage.

[48]  Andrew T. Smith,et al.  A comment on the severity of the effects of non-white noise in fMRI time-series , 2007, NeuroImage.

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

[50]  David Ress,et al.  Topography of covert visual attention in human superior colliculus. , 2010, Journal of neurophysiology.

[51]  E. Maylor,et al.  Inhibitory component of externally controlled covert orienting in visual space. , 1985, Journal of experimental psychology. Human perception and performance.

[52]  Hans-Jochen Heinze,et al.  High-Field fMRI Reveals Brain Activation Patterns Underlying Saccade Execution in the Human Superior Colliculus , 2010, PloS one.

[53]  Stephen D. Mayhew,et al.  Brainstem functional magnetic resonance imaging: Disentangling signal from physiological noise , 2008, Journal of magnetic resonance imaging : JMRI.

[54]  R. Klein,et al.  Contribution of the Primate Superior Colliculus to Inhibition of Return , 2002, Journal of Cognitive Neuroscience.

[55]  H Egeth,et al.  Inhibition and disinhibition of return: Evidence from temporal order judgments , 1994, Perception & psychophysics.

[56]  Andrew R. Mayer,et al.  An Event-related fMRI Study of Exogenous Orienting: Supporting Evidence for the Cortical Basis of Inhibition of Return? , 2004, Journal of Cognitive Neuroscience.

[57]  Sabine Kastner,et al.  Effects of Sustained Spatial Attention in the Human Lateral Geniculate Nucleus and Superior Colliculus , 2009, The Journal of Neuroscience.

[58]  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.

[59]  Raymond Klein,et al.  Inhibition of return , 2000, Trends in Cognitive Sciences.

[60]  B. Milliken,et al.  The manifestation of attentional capture: facilitation or IOR depending on task demands , 2007, Psychological research.

[61]  Avishai Henik,et al.  Parietal Lobe Lesions Disrupt Saccadic Remapping of Inhibitory Location Tagging , 2004, Journal of Cognitive Neuroscience.

[62]  David E. Irwin,et al.  Capturing attention , 1981, Cognition.

[63]  A. Sereno,et al.  Inhibition of return in manual and saccadic response systems , 2000, Perception & psychophysics.