Spatial attention increases the pupillary response to light changes.

We measured pupil size in adult human subjects while we manipulated both the luminance of the visual scene and the location of attention. We found that, with central fixation maintained, pupillary constrictions and dilations evoked by peripheral luminance increments and decrements are larger when spatial attention is covertly (i.e., with no eye movements) directed to the stimulus region versus when it is directed to the opposite hemifield. Irrespective of the size of the attended region (focused at the center of the stimulus or spread within and outside the stimulus), the attentional enhancement is large: more than 20% of the response to stimuli in the unattended hemifield. This indicates that a sizable portion of this simple ocular behavior—often considered a subcortical "reflex"—in fact depends on cortical processing. Together, these features indicate that pupillometry is not only an index of retinal and brainstem function, but also an objective measure of complex constructs such as attention and its effects on sensory processing.

[1]  C. Eriksen,et al.  Visual attention within and around the field of focal attention: A zoom lens model , 1986, Perception & psychophysics.

[2]  P. Tse Voluntary attention modulates the brightness of overlapping transparent surfaces , 2005, Vision Research.

[3]  T Rowan Candy,et al.  Pupil responses to near visual demand during human visual development. , 2011, Journal of vision.

[4]  D. Heeger,et al.  The Normalization Model of Attention , 2009, Neuron.

[5]  S. Sirois,et al.  Pupillometry , 2012, Perspectives on psychological science : a journal of the Association for Psychological Science.

[6]  Attenuation of the pupil response during binocular rivalry. , 1966, Vision research.

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

[8]  Rockefeller S. L. Young,et al.  Transient and sustained components of the pupillary responses evoked by luminance and color , 1993, Vision Research.

[9]  Paul D. Gamlin,et al.  The pupillary light reflex pathway of the primate. , 1995, Journal of the American Optometric Association.

[10]  Jean Lorenceau,et al.  Pupil dynamics during bistable motion perception. , 2009, Journal of vision.

[11]  Alex R. Wade,et al.  Differential attentional modulation of cortical responses to S-cone and luminance stimuli. , 2011, Journal of vision.

[12]  C. Koch,et al.  Pupil dilation reflects perceptual selection and predicts subsequent stability in perceptual rivalry , 2008, Proceedings of the National Academy of Sciences.

[13]  J. Grainger,et al.  The Pupillary Light Response Reveals the Focus of Covert Visual Attention , 2013, PloS one.

[14]  Rockefeller S. L. Young,et al.  Transient and sustained components of the pupil response evoked by achromatic spatial patterns , 1993, Vision Research.

[15]  Ken Nakayama,et al.  Pupil responses to high-level image content. , 2013, Journal of vision.

[16]  L. Kaufman,et al.  Handbook of perception and human performance , 1986 .

[17]  F. Campbell,et al.  Effect of Size of Pupil on Visual Acuity , 1960, Nature.

[18]  J. Pokorny,et al.  Human and macaque pupil responses driven by melanopsin-containing retinal ganglion cells , 2007, Vision Research.

[19]  R. Lucas,et al.  Mammalian Inner Retinal Photoreception , 2013, Current Biology.

[20]  E. Hess,et al.  Pupil Size as Related to Interest Value of Visual Stimuli , 1960, Science.

[21]  William Prinzmetal,et al.  The Phenomenology of Attention , 1997, Consciousness and Cognition.

[22]  B. Laeng,et al.  Bright illusions reduce the eye's pupil , 2012, Proceedings of the National Academy of Sciences.

[23]  G. Boynton A framework for describing the effects of attention on visual responses , 2009, Vision Research.

[24]  J. Barbur,et al.  Pupil response triggered by the onset of coherent motion , 1997, Graefe's Archive for Clinical and Experimental Ophthalmology.

[25]  Paola Binda,et al.  Pupil constrictions to photographs of the sun. , 2013, Journal of vision.

[26]  A. Treisman,et al.  A feature-integration theory of attention , 1980, Cognitive Psychology.

[27]  M. Posner,et al.  Orienting of Attention* , 1980, The Quarterly journal of experimental psychology.

[28]  Matthew F. Peterson,et al.  Statistical decision theory to relate neurons to behavior in the study of covert visual attention , 2009, Vision Research.

[29]  D Kahneman,et al.  Pupil Diameter and Load on Memory , 1966, Science.

[30]  B. Gilmartin,et al.  Absence of pupil response to blur-driven accommodation , 1992, Vision Research.

[31]  Paola Binda,et al.  Attention to Bright Surfaces Enhances the Pupillary Light Reflex , 2013, The Journal of Neuroscience.

[32]  B. L. Zuber,et al.  Suppression of the Pupillary Light Reflex in Binocular Rivalry and Saccadic Suppression , 1965, Nature.

[33]  I. E. Loewenfeld,et al.  The Pupil: Anatomy, Physiology, and Clinical Applications , 1999 .

[34]  B. L. Zuber,et al.  Saccadic suppression of the pupillary light reflex. , 1966, Experimental neurology.

[35]  B. Laeng,et al.  The Eye Pupil Adjusts to Imaginary Light , 2014, Psychological science.

[36]  T. Badea,et al.  Melanopsin cells are the principal conduits for rod–cone input to non-image-forming vision , 2008, Nature.

[37]  Stefan M. Wierda,et al.  Pupil dilation deconvolution reveals the dynamics of attention at high temporal resolution , 2012, Proceedings of the National Academy of Sciences.

[38]  Robert C. Wilson,et al.  Rational regulation of learning dynamics by pupil–linked arousal systems , 2012, Nature Neuroscience.

[39]  Joonyeol Lee,et al.  A Normalization Model of Attentional Modulation of Single Unit Responses , 2009, PloS one.

[40]  K. Yau,et al.  Diminished Pupillary Light Reflex at High Irradiances in Melanopsin-Knockout Mice , 2003, Science.

[41]  M. Carrasco Visual attention: The past 25 years , 2011, Vision Research.

[42]  M. Carrasco,et al.  Attention alters appearance , 2004, Nature Neuroscience.

[43]  L. Chalupa,et al.  The visual neurosciences , 2004 .

[44]  Helmut Wilhelm,et al.  Pupil response components: studies in patients with Parinaud's syndrome. , 2002, Brain : a journal of neurology.

[45]  K. Schneider,et al.  Attention biases decisions but does not alter appearance. , 2008, Journal of vision.

[46]  E MARG,et al.  The pupillary near reflex; the relation of pupillary diameter to accommodation and the various components of convergence. , 1949, American journal of optometry and archives of American Academy of Optometry.

[47]  Amy M. Ni,et al.  Tuned Normalization Explains the Size of Attention Modulations , 2012, Neuron.

[48]  Hannah E Smithson,et al.  Compatible and incompatible representations in visual sensory storage. , 2012, Journal of vision.

[49]  J L Barbur,et al.  Pupillary responses to stimulus structure, colour and movement , 1992, Ophthalmic & physiological optics : the journal of the British College of Ophthalmic Opticians.

[50]  Simon Barthelmé,et al.  Modeling fixation locations using spatial point processes. , 2012, Journal of vision.

[51]  D. Heeger,et al.  When size matters: attention affects performance by contrast or response gain , 2010, Nature Neuroscience.

[52]  M. Carandini,et al.  Normalization as a canonical neural computation , 2013, Nature Reviews Neuroscience.

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

[54]  P. Binda,et al.  Pupil size reflects the focus of feature-based attention. , 2014, Journal of neurophysiology.

[55]  J. Yellott,et al.  A unified formula for light-adapted pupil size. , 2012, Journal of vision.

[56]  Paul D. Gamlin,et al.  Behavior of luminance neurons in the pretectal olivary nucleus during the pupillary near response , 1996, Experimental Brain Research.