Spatial memory following shifts of gaze. I. Saccades to memorized world-fixed and gaze-fixed targets.

During a shift of gaze, an object can move along with gaze or stay fixed in the world. To examine the effect of an object's reference frame on spatial working memory, we trained monkeys to memorize locations of visual stimuli as either fixed in the world or fixed to gaze. Each trial consisted of an initial reference frame instruction, followed by a peripheral visual flash, a memory-period gaze shift, and finally a memory-guided saccade to the location consistent with the instructed reference frame. The memory-period gaze shift was either rapid (a saccade) or slow (smooth pursuit or whole body rotation). This design allowed a comparison of memory-guided saccade performance under various conditions. Our data indicate that after a rotation or smooth-pursuit eye movement, saccades to memorized world-fixed targets are more variable than saccades to memorized gaze-fixed targets. In contrast, memory-guided saccades to world- and gaze-fixed targets are equally variable following a visually guided saccade. Across all conditions, accuracy, latency, and main sequence characteristics of memory-guided saccades are not influenced by the target's reference frame. Memory-guided saccades are, however, more accurate after fast compared with slow gaze shifts. These results are most consistent with an eye-centered representational system for storing the spatial locations of memorized objects but suggest that the visual system may engage different mechanisms to update the stored signal depending on how gaze is shifted.

[1]  R. Andersen,et al.  Motor intention activity in the macaque's lateral intraparietal area. I. Dissociation of motor plan from sensory memory. , 1996, Journal of neurophysiology.

[2]  K Ohtsuka Properties of memory-guided saccades toward targets flashed during smooth pursuit in human subjects. , 1994, Investigative ophthalmology & visual science.

[3]  Kae Nakamura,et al.  Updating of the visual representation in monkey striate and extrastriate cortex during saccades , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[4]  M. Schlag-Rey,et al.  Through the eye, slowly; Delays and localization errors in the visual system , 2002, Nature Reviews Neuroscience.

[5]  C L Colby,et al.  Visual, saccade-related, and cognitive activation of single neurons in monkey extrastriate area V3A. , 2000, Journal of neurophysiology.

[6]  W Pieter Medendorp,et al.  Rotational Remapping in Human Spatial Memory during Eye and Head Motion , 2002, The Journal of Neuroscience.

[7]  M. Goldberg,et al.  Spatial processing in the monkey frontal eye field. I. Predictive visual responses. , 1997, Journal of neurophysiology.

[8]  J R Duhamel,et al.  The updating of the representation of visual space in parietal cortex by intended eye movements. , 1992, Science.

[9]  I Israël,et al.  Vestibular information contributes to update retinotopic maps. , 1999, Neuroreport.

[10]  B. Bridgeman,et al.  Immediate post-saccadic information mediates space constancy , 1998, Vision Research.

[11]  C. Bruce,et al.  Primate frontal eye fields. III. Maintenance of a spatially accurate saccade signal. , 1990, Journal of neurophysiology.

[12]  M. Schlag-Rey,et al.  Saccades can be aimed at the spatial location of targets flashed during pursuit. , 1990, Journal of neurophysiology.

[13]  E. M. Klier,et al.  Human oculomotor system accounts for 3-D eye orientation in the visual-motor transformation for saccades. , 1998, Journal of neurophysiology.

[14]  Hermann von Helmholtz,et al.  Treatise on Physiological Optics , 1962 .

[15]  E. Holst,et al.  Das Reafferenzprinzip , 2004, Naturwissenschaften.

[16]  W. Heide,et al.  Cortical control of double‐step saccades: Implications for spatial orientation , 1995, Annals of neurology.

[17]  M. Goldberg,et al.  Saccadic dysmetria in a patient with a right frontoparietal lesion. The importance of corollary discharge for accurate spatial behaviour. , 1992, Brain : a journal of neurology.

[18]  R. Andersen,et al.  The parietal reach region codes the next planned movement in a sequential reach task. , 2001, Journal of neurophysiology.

[19]  D Guitton,et al.  Human head-free gaze saccades to targets flashed before gaze-pursuit are spatially accurate. , 1998, Journal of neurophysiology.

[20]  D. Robinson,et al.  A METHOD OF MEASURING EYE MOVEMENT USING A SCLERAL SEARCH COIL IN A MAGNETIC FIELD. , 1963, IEEE transactions on bio-medical engineering.

[21]  M. Behrmann,et al.  Updating of locations during whole-body rotations in patients with hemispatial neglect , 2001, Cognitive, affective & behavioral neuroscience.

[22]  T Mergner,et al.  Vestibular memory‐contingent saccades involve somatosensory input from the body support , 1998, Neuroreport.

[23]  I. Israël,et al.  Vestibular perception of passive whole-body rotation about horizontal and vertical axes in humans: goal-directed vestibulo-ocular reflex and vestibular memory-contingent saccades , 2004, Experimental Brain Research.

[24]  F E Guedry,et al.  The influence of active versus passive head oscillation, and mental set on the human vestibulo-ocular reflex. , 1988, Aviation, space, and environmental medicine.

[25]  M. Hayhoe,et al.  Reference frames in saccadic targeting , 1997, Experimental Brain Research.

[26]  M. Hayhoe,et al.  Memory representations guide targeting eye movements in a natural task , 2000 .

[27]  Richard A. Andersen,et al.  A back-propagation programmed network that simulates response properties of a subset of posterior parietal neurons , 1988, Nature.

[28]  R. Andersen,et al.  Inactivation of macaque lateral intraparietal area delays initiation of the second saccade predominantly from contralesional eye positions in a double-saccade task , 2001, Experimental Brain Research.

[29]  B. Segal,et al.  Adaptive modification of vestibularly perceived rotation , 2004, Experimental Brain Research.

[30]  W. P. Medendorp,et al.  Pointing to remembered visual targets after active one-step self-displacements within reaching space , 1999, Experimental Brain Research.

[31]  T Vilis,et al.  A reexamination of the gain of the vestibuloocular reflex. , 1986, Journal of neurophysiology.

[32]  L. Snyder,et al.  Effect of viewing distance and location of the axis of head rotation on the monkey's vestibuloocular reflex. I. Eye movement responses. , 1992, Journal of neurophysiology.

[33]  L F Dell'Osso,et al.  Saccades to remembered targets: the effects of smooth pursuit and illusory stimulus motion. , 1996, Journal of neurophysiology.

[34]  L. Optican,et al.  Slow saccades in spinocerebellar degeneration. , 1976, Archives of neurology.

[35]  A. Berthoz,et al.  Reaching beyond reach , 1999, Experimental Brain Research.

[36]  D. Sparks,et al.  Spatial localization of saccade targets. I. Compensation for stimulation-induced perturbations in eye position. , 1983, Journal of neurophysiology.

[37]  R. Wurtz,et al.  A Pathway in Primate Brain for Internal Monitoring of Movements , 2002, Science.

[38]  H Honda,et al.  The extraretinal signal from the pursuit-eye-movement system: Its role in the perceptual and the egocentric localization systems , 1990, Perception & psychophysics.

[39]  L. Stark,et al.  Role of corollary discharge in space constancy , 1983, Perception & psychophysics.

[40]  P. E. Hallett,et al.  Saccadic eye movements towards stimuli triggered by prior saccades , 1976, Vision Research.

[41]  B. Richmond,et al.  Implantation of magnetic search coils for measurement of eye position: An improved method , 1980, Vision Research.

[42]  L. Stark,et al.  The main sequence, a tool for studying human eye movements , 1975 .

[43]  P. Medendorp,et al.  Visuospatial updating of reaching targets in near and far space , 2002, Neuroreport.

[44]  S. Black,et al.  Intact spatial updating during locomotion after right posterior parietal lesions , 2000, Neuropsychologia.

[45]  M. Goldberg,et al.  The visual and frontal cortices. , 1989, Reviews of oculomotor research.

[46]  M. Goldberg,et al.  Neurons in the monkey superior colliculus predict the visual result of impending saccadic eye movements. , 1995, Journal of neurophysiology.

[47]  L. Fogassi,et al.  Eye position effects on visual, memory, and saccade-related activity in areas LIP and 7a of macaque , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.