Visual sensitivity of frontal eye field neurons during the preparation of saccadic eye movements.

Primate vision is continuously disrupted by saccadic eye movements, and yet this disruption goes unperceived. One mechanism thought to reduce perception of this self-generated movement is saccadic suppression, a global loss of visual sensitivity just before, during, and after saccadic eye movements. The frontal eye field (FEF) is a candidate source of neural correlates of saccadic suppression previously observed in visual cortex, because it contributes to the generation of visually guided saccades and modulates visual cortical responses. However, whether the FEF exhibits a perisaccadic reduction in visual sensitivity that could be transmitted to visual cortex is unknown. To determine whether the FEF exhibits a signature of saccadic suppression, we recorded the visual responses of FEF neurons to brief, full-field visual probe stimuli presented during fixation and before onset of saccades directed away from the receptive field in rhesus macaques (Macaca mulatta) We measured visual sensitivity during both epochs and found that it declines before saccade onset. Visual sensitivity was significantly reduced in visual but not visuomotor neurons. This reduced sensitivity was also present in visual neurons with no movement-related modulation during visually guided saccades and thus occurred independently from movement-related activity. Across the population of visual neurons, sensitivity began declining ∼80 ms before saccade onset. We also observed a similar presaccadic reduction in sensitivity to isoluminant, chromatic stimuli. Our results demonstrate that the signaling of visual information by FEF neurons is reduced during saccade preparation, and thus these neurons exhibit a signature of saccadic suppression.

[1]  P. Cavanagh,et al.  Saccadic suppression of low-level motion , 1989, Vision Research.

[2]  M. Ibbotson,et al.  Enhanced motion sensitivity follows saccadic suppression in the superior temporal sulcus of the macaque cortex. , 2006, Cerebral cortex.

[3]  P. Roelfsema,et al.  Modulation of the Contrast Response Function by Electrical Microstimulation of the Macaque Frontal Eye Field , 2009, The Journal of Neuroscience.

[4]  D. Burr,et al.  Selective depression of motion sensitivity during saccades. , 1982, The Journal of physiology.

[5]  J. Bullier,et al.  Topography of visual cortex connections with frontal eye field in macaque: convergence and segregation of processing streams , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[6]  Wilsaan M. Joiner,et al.  Suppressive Surrounds of Receptive Fields In Monkey Frontal Eye Field , 2012, The Journal of Neuroscience.

[7]  C. Bruce,et al.  Primate frontal eye fields. I. Single neurons discharging before saccades. , 1985, Journal of neurophysiology.

[8]  B. C. Motter,et al.  Modulation of Transient and Sustained Response Components of V4 Neurons by Temporal Crowding in Flashed Stimulus Sequences , 2006, The Journal of Neuroscience.

[9]  G. Rhodes,et al.  Sex-specific norms code face identity. , 2011, Journal of vision.

[10]  N. P. Bichot,et al.  Perceptual and motor processing stages identified in the activity of macaque frontal eye field neurons during visual search. , 1996, Journal of neurophysiology.

[11]  D. E.Vonholstan,et al.  The Principle of Reafference : Interactions Between the Central Nervous System and the Peripheral Organs , 2011 .

[12]  Katherine M. Armstrong,et al.  Selective gating of visual signals by microstimulation of frontal cortex , 2003, Nature.

[13]  J Schlag,et al.  Interaction of the two frontal eye fields before saccade onset. , 1998, Journal of neurophysiology.

[14]  Nicholas A. Steinmetz,et al.  Visual Space is Compressed in Prefrontal Cortex Before Eye Movements , 2014, Nature.

[15]  K. Hoffmann,et al.  Neural Dynamics of Saccadic Suppression , 2009, Journal of Neuroscience.

[16]  R. Wurtz,et al.  Enhancement of visual responses in monkey striate cortex and frontal eye fields. , 1976, Journal of neurophysiology.

[17]  D. Burr,et al.  Contrast sensitivity at high velocities , 1982, Vision Research.

[18]  Frank Bremmer,et al.  Spatiotemporal profile of peri-saccadic contrast sensitivity. , 2011, Journal of vision.

[19]  B. L. Zuber,et al.  Saccadic suppression: elevation of visual threshold associated with saccadic eye movements. , 1966, Experimental neurology.

[20]  Nicholas A. Steinmetz,et al.  Frontal eye field , 2012, Scholarpedia.

[21]  M. Morrone,et al.  Extraretinal Control of Saccadic Suppression , 2000, The Journal of Neuroscience.

[22]  Tirin Moore,et al.  Influence and Limitations of Popout in the Selection of Salient Visual Stimuli by Area V4 Neurons , 2009, The Journal of Neuroscience.

[23]  C. Legéndy,et al.  Bursts and recurrences of bursts in the spike trains of spontaneously active striate cortex neurons. , 1985, Journal of neurophysiology.

[24]  W. D. Wright Physiological Optics , 1958, Nature.

[25]  T. Moore,et al.  CONTROL OF VISUAL CORTICAL SIGNALS BY PREFRONTAL DOPAMINE , 2011, Nature.

[26]  R. Sperry Neural basis of the spontaneous optokinetic response produced by visual inversion. , 1950, Journal of comparative and physiological psychology.

[27]  G. Horwitz,et al.  Effects of microsaccades on contrast detection and V 1 responses in macaques Program in Neurobiology and Behavior , 2011 .

[28]  Henry Kennedy,et al.  Pathways of Attention: Synaptic Relationships of Frontal Eye Field to V4, Lateral Intraparietal Cortex, and Area 46 in Macaque Monkey , 2011, The Journal of Neuroscience.

[29]  Robert H. Wurtz,et al.  Signals Conveyed in the Pulvinar Pathway from Superior Colliculus to Cortical Area MT , 2011, The Journal of Neuroscience.

[30]  R. Wurtz,et al.  Frontal eye field neurons orthodromically activated from the superior colliculus. , 1998, Journal of neurophysiology.

[31]  Robert H. Wurtz,et al.  Compression and Suppression of Shifting Receptive Field Activity in Frontal Eye Field Neurons , 2013, The Journal of Neuroscience.

[32]  R. Wurtz,et al.  Use of an extraretinal signal by monkey superior colliculus neurons to distinguish real from self-induced stimulus movement. , 1976, Journal of neurophysiology.

[33]  M. Ibbotson,et al.  Visual perception and saccadic eye movements , 2011, Current Opinion in Neurobiology.

[34]  R. Reid,et al.  Saccadic Eye Movements Modulate Visual Responses in the Lateral Geniculate Nucleus , 2002, Neuron.

[35]  Tirin Moore,et al.  Dynamic sensitivity of area V4 neurons during saccade preparation , 2009, Proceedings of the National Academy of Sciences.

[36]  Bart Krekelberg,et al.  Neural Correlates of Saccadic Suppression in Humans , 2004, Current Biology.

[37]  D. Burr,et al.  Selective suppression of the magnocellular visual pathway during saccadic eye movements , 1994, Nature.

[38]  Ziad M. Hafed,et al.  Microsaccadic Suppression of Visual Bursts in the Primate Superior Colliculus , 2010, Journal of Neuroscience.

[39]  Marc A Sommer,et al.  Neuronal adaptation caused by sequential visual stimulation in the frontal eye field. , 2008, Journal of neurophysiology.

[40]  P. H. Schiller Single unit analysis of backward visual masking and metacontrast in the cat lateral geniculate nucleus. , 1968, Vision research.

[41]  A. Leventhal,et al.  Signal timing across the macaque visual system. , 1998, Journal of neurophysiology.

[42]  D. M. Green,et al.  Signal detection theory and psychophysics , 1966 .

[43]  David L. Sheinberg,et al.  Noticing Familiar Objects in Real World Scenes: The Role of Temporal Cortical Neurons in Natural Vision , 2001, The Journal of Neuroscience.

[44]  K. Hoffmann,et al.  Neural Mechanisms of Saccadic Suppression , 2002, Science.

[45]  M. W. Brown,et al.  Neuronal evidence that inferomedial temporal cortex is more important than hippocampus in certain processes underlying recognition memory , 1987, Brain Research.

[46]  C. Bruce,et al.  Primate frontal eye fields. II. Physiological and anatomical correlates of electrically evoked eye movements. , 1985, Journal of neurophysiology.

[47]  David W. Royal,et al.  Correlates of motor planning and postsaccadic fixation in the macaque monkey lateral geniculate nucleus , 2005, Experimental Brain Research.

[48]  P. Latour Visual threshold during eye movements , 1962 .

[49]  M. Sommer,et al.  Neuronal adaptation due to sequential visual stimulation in the frontal eye field , 2008 .

[50]  Tirin Moore,et al.  Changes in Visual Receptive Fields with Microstimulation of Frontal Cortex , 2006, Neuron.

[51]  G. Rees,et al.  Saccades Differentially Modulate Human LGN and V1 Responses in the Presence and Absence of Visual Stimulation , 2005, Current Biology.

[52]  M. Schlag-Rey,et al.  How the frontal eye field can impose a saccade goal on superior colliculus neurons. , 1992, Journal of neurophysiology.

[53]  Tirin Moore,et al.  The Influence of Gaze Control on Visual Perception: Eye Movements and Visual Stability. , 2014, Cold Spring Harbor symposia on quantitative biology.

[54]  C. Bruce,et al.  Topography of projections to posterior cortical areas from the macaque frontal eye fields , 1995, The Journal of comparative neurology.

[55]  Tirin Moore,et al.  A Distinct Contribution of the Frontal Eye Field to the Visual Representation of Saccadic Targets , 2014, The Journal of Neuroscience.

[56]  J. Movshon,et al.  The analysis of visual motion: a comparison of neuronal and psychophysical performance , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[57]  J. Schall Neuronal activity related to visually guided saccades in the frontal eye fields of rhesus monkeys: comparison with supplementary eye fields. , 1991, Journal of neurophysiology.