Functional distinction between visuomovement and movement neurons in macaque frontal eye field during saccade countermanding.

In the previous studies on the neural control of saccade initiation using the countermanding paradigm, movement and visuomovement neurons in the frontal eye field were grouped as movement-related neurons. The activity of both types of neurons was modulated when a saccade was inhibited in response to a stop signal, and this modulation occurred early enough to contribute to the control of the saccade initiation. We now report a functional difference between these two classes of neurons when saccades are produced. Movement neurons exhibited a progressive accumulation of discharge rate following target presentation that triggered a saccade when it reached a threshold. When saccades were inhibited with lower probability in response to a stop signal appearing at longer delays, this accumulating activity was interrupted at levels progressively closer to the threshold. In contrast, visuomovement neurons exhibited a maintained elevated discharge rate following target presentation that was followed by a further enhancement immediately before the saccade initiation. When saccades were inhibited in response to a stop signal, the late enhancement was absent and the maintained activity decayed regardless of stop-signal delay. These results demonstrate that the activity of movement neurons realizes the progressive commitment to the saccade initiation modeled by the activation of the go unit in computational models of countermanding performance. The lack of correspondence of the activity of visuomovement neurons with any elements of these models indicates that visuomovement neurons perform a function other than the saccade preparation such as a corollary discharge to update visual processing.

[1]  J. Schall,et al.  Role of frontal eye fields in countermanding saccades: visual, movement, and fixation activity. , 1998, Journal of neurophysiology.

[2]  D. P. Hanes,et al.  Controlled Movement Processing: Superior Colliculus Activity Associated with Countermanded Saccades , 2003, The Journal of Neuroscience.

[3]  Pierre Pouget,et al.  Attentional selection during preparation of eye movements , 2004, Psychological research.

[4]  H. Honda Perceptual localization of visual stimuli flashed during saccades , 1989, Perception & psychophysics.

[5]  I. Franks,et al.  A horse race between independent processes : Evidence for a phantom point of no return in the preparation of a speeded motor response , 1997 .

[6]  D. Munoz,et al.  Control of saccade initiation in a countermanding task using visual and auditory stop signals , 2000, Experimental Brain Research.

[7]  J. Schlag,et al.  Illusory localization of stimuli flashed in the dark before saccades , 1995, Vision Research.

[8]  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.

[9]  J. Hoffman,et al.  The role of visual attention in saccadic eye movements , 1995, Perception & psychophysics.

[10]  M E Goldberg,et al.  Participation of prefrontal neurons in the preparation of visually guided eye movements in the rhesus monkey. , 1989, Journal of neurophysiology.

[11]  J. Schall,et al.  Neural Control of Voluntary Movement Initiation , 1996, Science.

[12]  Aditya Murthy,et al.  Neural control of visual search by frontal eye field: effects of unexpected target displacement on visual selection and saccade preparation. , 2009, Journal of neurophysiology.

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

[14]  D. E. Irwin,et al.  Covert shifts of attention precede involuntary eye movements. , 2010, Perception & psychophysics.

[15]  Brian D Corneil,et al.  A "gap effect" on stop signal reaction times in a human saccadic countermanding task. , 2009, Journal of neurophysiology.

[16]  D. Burr,et al.  Temporal Impulse Response Functions for Luminance and Colour During Saccades , 1996, Vision Research.

[17]  M. Shadlen,et al.  Decision-making with multiple alternatives , 2008, Nature Neuroscience.

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

[19]  David E. Irwin,et al.  Don’t look! don’t touch! inhibitory control of eye and hand movements , 2000, Psychonomic bulletin & review.

[20]  F. C. Volkmann Human visual suppression , 1986, Vision Research.

[21]  Hans Colonius,et al.  Countermanding saccades with auditory stop signals: testing the race model , 2001, Vision Research.

[22]  M. Goldberg,et al.  Rhesus monkeys mislocalize saccade targets flashed for 100ms around the time of a saccade , 2007, Vision Research.

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

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

[25]  P Dassonville,et al.  Oculomotor localization relies on a damped representation of saccadic eye displacement in human and nonhuman primates , 1992, Visual Neuroscience.

[26]  G. Rizzolatti Mechanisms of Selective Attention in Mammals , 1983 .

[27]  B. Fischer,et al.  Peripheral attention versus central fixation: Modulation of the visual activity of prelunate cortical cells of the rhesus monkey , 1985, Brain Research.

[28]  G. Logan,et al.  In search of the point of no return: the control of response processes. , 1990, Journal of experimental psychology. Human perception and performance.

[29]  D. Munoz,et al.  Inhibitory control of eye movements during oculomotor countermanding in adults with attention-deficit hyperactivity disorder , 2003, Experimental Brain Research.

[30]  D. E. Irwin,et al.  Covert shifts of attention precede involuntary eye movements , 2004 .

[31]  T. Moore,et al.  Presaccadic discrimination of receptive field stimuli by area V4 neurons , 2009, Vision Research.

[32]  A. Kingstone,et al.  Fixation offset and stop signal intensity effects on saccadic countermanding: a crossmodal investigation , 2006, Experimental Brain Research.

[33]  B. Fischer,et al.  Enhanced activation of neurons in prelunate cortex before visually guided saccades of trained rhesus monkeys , 2004, Experimental Brain Research.

[34]  L A Krubitzer,et al.  Frontal eye field as defined by intracortical microstimulation in squirrel monkeys, owl monkeys, and macaque monkeys II. cortical connections , 1986, The Journal of comparative neurology.

[35]  J. Findlay,et al.  The Relationship between Eye Movements and Spatial Attention , 1986, The Quarterly journal of experimental psychology. A, Human experimental psychology.

[36]  M. Goldberg,et al.  Visual, presaccadic, and cognitive activation of single neurons in monkey lateral intraparietal area. , 1996, Journal of neurophysiology.

[37]  R. Wurtz,et al.  Brain circuits for the internal monitoring of movements. , 2008, Annual review of neuroscience.

[38]  D. Burr,et al.  Changes in visual perception at the time of saccades , 2001, Trends in Neurosciences.

[39]  J. Schall,et al.  Countermanding saccades in macaque , 1995, Visual Neuroscience.

[40]  M. J. Friedlander,et al.  The time course and amplitude of EPSPs evoked at synapses between pairs of CA3/CA1 neurons in the hippocampal slice , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[41]  R. Carpenter,et al.  Countermanding saccades in humans , 1999, Vision Research.

[42]  H. Deubel,et al.  Saccade target selection and object recognition: Evidence for a common attentional mechanism , 1996, Vision Research.

[43]  Chung-Chuan Lo,et al.  Proactive Inhibitory Control and Attractor Dynamics in Countermanding Action: A Spiking Neural Circuit Model , 2009, The Journal of Neuroscience.

[44]  E. J. Tehovnik,et al.  Eye Movements Modulate Visual Receptive Fields of V4 Neurons , 2001, Neuron.

[45]  A. Kingstone,et al.  Topic: Cognition , 2003 .

[46]  Afferent delays and the mislocalization of perisaccadic stimuli , 2001, Vision Research.

[47]  D. Meyer,et al.  The point of no return in choice reaction time: controlled and ballistic stages of response preparation. , 1986, Journal of experimental psychology. Human perception and performance.

[48]  Markus Lappe,et al.  Effect of saccadic adaptation on localization of visual targets. , 2005, Journal of neurophysiology.

[49]  J. Henderson,et al.  Stimulus discrimination following covert attentional orienting to an exogenous cue. , 1991, Journal of experimental psychology. Human perception and performance.

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

[51]  Joshua W. Brown,et al.  Relation of frontal eye field activity to saccade initiation during a countermanding task , 2008, Experimental Brain Research.

[52]  Jeremiah Y. Cohen,et al.  The neural basis of saccade target selection , 1995 .

[53]  T Moore,et al.  Shape representations and visual guidance of saccadic eye movements. , 1999, Science.

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

[55]  Hans Colonius,et al.  Countermanding saccades: Evidence against independent processing of go and stop signals , 2003, Perception & psychophysics.

[56]  Neeraj J Gandhi,et al.  Behavioral evaluation of movement cancellation. , 2006, Journal of neurophysiology.

[57]  P H Schiller,et al.  Visual representations during saccadic eye movements. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[58]  J. Schall,et al.  Visual and Motor Connectivity and the Distribution of Calcium-Binding Proteins in Macaque Frontal Eye Field: Implications for Saccade Target Selection , 2009, Front. Neuroanat..

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

[60]  Carrie J. McAdams,et al.  Effects of Attention on Orientation-Tuning Functions of Single Neurons in Macaque Cortical Area V4 , 1999, The Journal of Neuroscience.

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

[62]  Robert H. Wurtz,et al.  Influence of the thalamus on spatial visual processing in frontal cortex , 2006, Nature.

[63]  R. Wurtz,et al.  What the brain stem tells the frontal cortex. I. Oculomotor signals sent from superior colliculus to frontal eye field via mediodorsal thalamus. , 2004, Journal of neurophysiology.

[64]  G. Rizzolatti,et al.  Orienting of attention and eye movements , 2004, Experimental Brain Research.

[65]  J. Reynolds,et al.  Attentional modulation of visual processing. , 2004, Annual review of neuroscience.

[66]  Toshio Iijima,et al.  Dual Transneuronal Tracing in the Rat Entorhinal-Hippocampal Circuit by Intracerebral Injection of Recombinant Rabies Virus Vectors , 2008, Front. Neuroanat..

[67]  Richard P. Heitz,et al.  Biophysical support for functionally distinct cell types in the frontal eye field. , 2009, Journal of neurophysiology.

[68]  G. Logan,et al.  Inhibitory control in mind and brain: an interactive race model of countermanding saccades. , 2007, Psychological review.

[69]  Aditya Murthy,et al.  Frontal eye field contributions to rapid corrective saccades. , 2007, Journal of neurophysiology.

[70]  G. Logan On the ability to inhibit thought and action , 1984 .

[71]  M. Shadlen,et al.  Response of Neurons in the Lateral Intraparietal Area during a Combined Visual Discrimination Reaction Time Task , 2002, The Journal of Neuroscience.

[72]  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.

[73]  S. Petersen,et al.  Saccade-related and visual activities in the pulvinar nuclei of the behaving rhesus monkey , 1986, Experimental Brain Research.

[74]  Marcus Kaiser,et al.  Perisaccadic Mislocalization Orthogonal to Saccade Direction , 2004, Neuron.

[75]  I M Franks,et al.  A horse race between independent processes: evidence for a phantom point of no return in preparation of a speeded motor response. , 1997, Journal of experimental psychology. Human perception and performance.

[76]  F. Bartlett Thinking: An Experimental and Social Study , 1958 .

[77]  B. Dosher,et al.  The role of attention in the programming of saccades , 1995, Vision Research.