Expansion of Direction Space around the Cardinal Axes Revealed by Smooth Pursuit Eye Movements

It is well established that perceptual direction discrimination shows an oblique effect; thresholds are higher for motion along diagonal directions than for motion along cardinal directions. Here, we compare simultaneous direction judgments and pursuit responses for the same motion stimuli and find that both pursuit and perceptual thresholds show similar anisotropies. The pursuit oblique effect is robust under a wide range of experimental manipulations, being largely resistant to changes in trajectory (radial versus tangential motion), speed (10 versus 25 deg/s), directional uncertainty (blocked versus randomly interleaved), and cognitive state (tracking alone versus concurrent tracking and perceptual tasks). Our data show that the pursuit oblique effect is caused by an effective expansion of direction space surrounding the cardinal directions and the requisite compression of space for other directions. This expansion suggests that the directions around the cardinal directions are in some way overrepresented in the visual cortical pathways that drive both smooth pursuit and perception.

[1]  Martin J. Steinbach,et al.  Pursuing the perceptual rather than the retinal stimulus , 1976, Vision Research.

[2]  R. Krauzlis,et al.  Shared motion signals for human perceptual decisions and oculomotor actions. , 2003, Journal of vision.

[3]  R. Andersen,et al.  Posterior parietal cortex. , 1989, Reviews of oculomotor research.

[4]  H. Komatsu,et al.  Relation of cortical areas MT and MST to pursuit eye movements. I. Localization and visual properties of neurons. , 1988, Journal of neurophysiology.

[5]  D. W. Heeley,et al.  Directional acuity for drifting plaids , 1992, Vision Research.

[6]  Constance S. Royden,et al.  Motion perception , 1998 .

[7]  Dominic Palmer-Brown,et al.  Illusions in action , 2001, Trends in Cognitive Sciences.

[8]  R J Krauzlis,et al.  Effects of directional expectations on motion perception and pursuit eye movements , 2001, Visual Neuroscience.

[9]  S Celebrini,et al.  Microstimulation of extrastriate area MST influences performance on a direction discrimination task. , 1995, Journal of neurophysiology.

[10]  Frederick A. Miles,et al.  Linking eye movements and perception , 2003 .

[11]  M. Goodale,et al.  Separate visual pathways for perception and action , 1992, Trends in Neurosciences.

[12]  W. Newsome,et al.  Deficits in visual motion processing following ibotenic acid lesions of the middle temporal visual area of the macaque monkey , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[13]  R. Mansfield,et al.  Analysis of visual behavior , 1982 .

[14]  W. Merigan,et al.  Motion perception following lesions of the superior temporal sulcus in the monkey. , 1994, Cerebral cortex.

[15]  P. Thier,et al.  Visual tracking neurons in primate area MST are activated by smooth-pursuit eye movements of an "imaginary" target. , 2003, Journal of neurophysiology.

[16]  Eileen Kowler,et al.  Sensitivity of smooth eye movement to small differences in target velocity , 1987, Vision Research.

[17]  Brent R. Beutter,et al.  Human motion perception and smooth eye movements slow similar directional biases for elongated apertures , 1998, Vision Research.

[18]  W. Newsome,et al.  A selective impairment of motion perception following lesions of the middle temporal visual area (MT) , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[19]  Raymond H. Cuijpers,et al.  Illusions in action: consequences of inconsistent processing of spatial attributes , 2002, Experimental Brain Research.

[20]  W. Newsome,et al.  Microstimulation in visual area MT: effects on direction discrimination performance , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[21]  H. Komatsu,et al.  Modulation of pursuit eye movements by stimulation of cortical areas MT and MST. , 1989, Journal of neurophysiology.

[22]  H. Komatsu,et al.  Relation of cortical areas MT and MST to pursuit eye movements. II. Differentiation of retinal from extraretinal inputs. , 1988, Journal of neurophysiology.

[23]  B. L. Gros,et al.  Anisotropies in visual motion perception: a fresh look. , 1998, Journal of the Optical Society of America. A, Optics, image science, and vision.

[24]  P. Thier,et al.  Posterior Parietal Cortex Neurons Encode Target Motion in World-Centered Coordinates , 2004, Neuron.

[25]  R. Sekuler,et al.  Direction-specific improvement in motion discrimination , 1987, Vision Research.

[26]  Bruce Bridgeman,et al.  The induced Roelofs effect: two visual systems or the shift of a single reference frame? , 2004, Vision Research.

[27]  Brent R Beutter,et al.  Human discrimination of visual direction of motion with and without smooth pursuit eye movements. , 2003, Journal of vision.

[28]  T. Pasternak,et al.  Transient and permanent deficits in motion perception after lesions of cortical areas MT and MST in the macaque monkey. , 1999, Cerebral cortex.

[29]  L S Stone,et al.  Motion coherence affects human perception and pursuit similarly , 2000, Visual Neuroscience.

[30]  T D Albright,et al.  Perceptual, Oculomotor, and Neural Responses to Moving Color Plaids , 1998, Perception.

[31]  R. Krauzlis,et al.  Tracking with the mind’s eye , 1999, Trends in Neurosciences.

[32]  M. Goodale,et al.  Visual control of action but not perception requires analytical processing of object shape , 2003, Nature.

[33]  Leslie G. Ungerleider Two cortical visual systems , 1982 .

[34]  G. Barnes,et al.  The role of expectancy and volition in smooth pursuit eye movements. , 2002, Progress in brain research.

[35]  S. Lisberger,et al.  Visual responses of Purkinje cells in the cerebellar flocculus during smooth-pursuit eye movements in monkeys. I. Simple spikes. , 1990, Journal of neurophysiology.

[36]  R. Wurtz,et al.  Pursuit and optokinetic deficits following chemical lesions of cortical areas MT and MST. , 1988, Journal of neurophysiology.

[37]  Stephen J Heinen,et al.  Human smooth pursuit direction discrimination , 1999, Vision Research.

[38]  Stephen G. Lisberger,et al.  Directional Anisotropies Reveal a Functional Segregation of Visual Motion Processing for Perception and Action , 2003, Neuron.

[39]  S. Lisberger,et al.  Properties of visual inputs that initiate horizontal smooth pursuit eye movements in monkeys , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[40]  E. J. Morris,et al.  Visual motion processing and sensory-motor integration for smooth pursuit eye movements. , 1987, Annual review of neuroscience.

[41]  Eileen Kowler Cognitive expectations, not habits, control anticipatory smooth oculomotor pursuit , 1989, Vision Research.

[42]  Richard J Krauzlis,et al.  Pursuit of the ineffable: perceptual and motor reversals during the tracking of apparent motion. , 2003, Journal of Vision.

[43]  J Lorenceau,et al.  Visual Motion Integration for Perception and Pursuit , 2000, Perception.