The Effect of FEF Microstimulation on the Responses of Neurons in the Lateral Intraparietal Area

The macaque FEFs and the lateral intraparietal area (LIP) are high-level cortical areas involved in both spatial attention and oculomotor behavior. Stimulating FEF at a level below the threshold for evoking saccades increases fMRI activity and gamma power in area LIP, but the precise effect exerted by the FEF on LIP neurons is unknown. In our study, we recorded LIP single-unit activity during a visually guided saccade task with a peripherally presented go signal during microstimulation of FEF. We found that FEF microstimulation increased the LIP spike rate immediately after the highly salient go signal inside the LIP receptive field when both target and go signal were presented inside the receptive field, and no other possible go cues were present on the screen. The effect of FEF microstimulation on the LIP response was positive until at least 800 msec after microstimulation had ceased, but reversed for longer trial durations. Therefore, FEF microstimulation can modulate the LIP spike rate only when attention is selectively directed toward the stimulated location. These results provide the first direct evidence for LIP spike rate modulations caused by FEF microstimulation, thus showing that FEF activity can be the source of top–down control of area LIP.

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

[2]  Jay A. Hennig,et al.  Signal Multiplexing and Single-Neuron Computations in Lateral Intraparietal Area During Decision-Making , 2013, The Journal of Neuroscience.

[3]  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.

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

[5]  Suliann Ben Hamed,et al.  A Functional Hierarchy within the Parietofrontal Network in Stimulus Selection and Attention Control , 2013, The Journal of Neuroscience.

[6]  Peter Janssen,et al.  Frontal eye field microstimulation induces task-dependent gamma oscillations in the lateral intraparietal area. , 2012, Journal of neurophysiology.

[7]  E. J. Tehovnik.  Electrical stimulation of neural tissue to evoke behavioral responses , 1996, Journal of Neuroscience Methods.

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

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

[10]  R. Wurtz,et al.  Comparison of cortico-cortical and cortico-collicular signals for the generation of saccadic eye movements. , 2002, Journal of neurophysiology.

[11]  J. Duhamel,et al.  The relationship between spatial attention and saccades in the frontoparietal network of the monkey , 2011, The European journal of neuroscience.

[12]  D. Gitelman,et al.  Covert Visual Spatial Orienting and Saccades: Overlapping Neural Systems , 2000, NeuroImage.

[13]  W. Vanduffel,et al.  Functional Heterogeneity of Macaque Lateral Intraparietal Neurons , 2011, The Journal of Neuroscience.

[14]  P. Roelfsema,et al.  Bottom-Up Dependent Gating of Frontal Signals in Early Visual Cortex , 2008, Science.

[15]  T Moore,et al.  Control of eye movements and spatial attention. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[16]  Earl K Miller,et al.  Cortical circuits for the control of attention , 2012, Current Opinion in Neurobiology.

[17]  J. Gottlieb.  Parietal mechanisms of target representation , 2002, Current Opinion in Neurobiology.

[18]  M. Shadlen,et al.  A representation of the hazard rate of elapsed time in macaque area LIP , 2005, Nature Neuroscience.

[19]  R. Andersen,et al.  Coding of intention in the posterior parietal cortex , 1997, Nature.

[20]  Etienne Olivier,et al.  Contribution of the Monkey Frontal Eye Field to Covert Visual Attention , 2006, The Journal of Neuroscience.

[21]  M. Corbetta,et al.  A Common Network of Functional Areas for Attention and Eye Movements , 1998, Neuron.

[22]  W. Newsome,et al.  Local Field Potential in Cortical Area MT: Stimulus Tuning and Behavioral Correlations , 2006, The Journal of Neuroscience.

[23]  Peter Janssen,et al.  FEF-microstimulation causes task-dependent modulation of occipital fMRI activity , 2013, NeuroImage.

[24]  Y. Miyashita,et al.  Functional Magnetic Resonance Imaging of Macaque Monkeys Performing Visually Guided Saccade Tasks Comparison of Cortical Eye Fields with Humans , 2004, Neuron.

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

[26]  M. Goldberg,et al.  Neuronal Activity in the Lateral Intraparietal Area and Spatial Attention , 2003, Science.

[27]  Junying Yuan,et al.  Selective gating of visual signals by microstimulation of frontal cortex , 2022 .

[28]  Etienne Olivier,et al.  A Deficit in Covert Attention after Parietal Cortex Inactivation in the Monkey , 2004, Neuron.

[29]  M. Goldberg,et al.  Space and attention in parietal cortex. , 1999, Annual review of neuroscience.

[30]  M. Goldberg,et al.  Representation of visuomotor space in the parietal lobe of the monkey. , 1990, Cold Spring Harbor symposia on quantitative biology.

[31]  B Suresh Krishna,et al.  Surround Suppression Sharpens the Priority Map in the Lateral Intraparietal Area , 2022 .

[32]  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.

[33]  R. Desimone,et al.  Attention Increases Sensitivity of V4 Neurons , 2000, Neuron.

[34]  M. Goldberg,et al.  Attention, intention, and priority in the parietal lobe. , 2010, Annual review of neuroscience.

[35]  T. Moore,et al.  Microstimulation of the frontal eye field and its effects on covert spatial attention. , 2004, Journal of neurophysiology.

[36]  C. Bruce,et al.  Suppression of task-related saccades by electrical stimulation in the primate's frontal eye field. , 1997, Journal of neurophysiology.

[37]  E. Miller,et al.  Response to Comment on "Top-Down Versus Bottom-Up Control of Attention in the Prefrontal and Posterior Parietal Cortices" , 2007, Science.

[38]  P. Goldman-Rakic,et al.  Inactivation of parietal and prefrontal cortex reveals interdependence of neural activity during memory-guided saccades. , 2000, Journal of neurophysiology.

[39]  J. Maunsell,et al.  Different Origins of Gamma Rhythm and High-Gamma Activity in Macaque Visual Cortex , 2011, PLoS biology.

[40]  Peter Janssen,et al.  Local Field Potential Activity Associated with Temporal Expectations in the Macaque Lateral Intraparietal Area , 2012, Journal of Cognitive Neuroscience.

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

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

[43]  Bruce R. Rosen,et al.  Optogenetically Induced Behavioral and Functional Network Changes in Primates , 2012, Current Biology.