Inhibitory Control and the Frontal Eye Fields

Inhibitory control mechanisms are important in a range of behaviors to prevent execution of motor acts which, having been planned, are no longer necessary. Ready examples of this can be seen in a range of sports, such as cricket and baseball, where the choice between execution or inhibition of a bat swing must be made in a brief time interval. The role of the FEFs, an area typically described in relation to eye movement functions but also involved in visual processes, was investigated in an inhibitory control task using transcranial magnetic stimulation (TMS). A stop signal task with manual responses was used, providing measures of impulsivity and inhibitory control. TMS over FEF had no effect on response generation (impulsivity, indexed by go signal RT) but disrupted inhibitory control (indexed by stop signal RT). This is the first demonstration of a role for FEF in this type of task in normal subjects in a task which did not require eye movements and complements previous TMS findings of roles for pre-SMA and inferior frontal gyrus (IFG) in inhibitory control.

[1]  J. Mattingley,et al.  Dissociable mechanisms of cognitive control in prefrontal and premotor cortex. , 2007, Journal of neurophysiology.

[2]  Clayton E Curtis,et al.  Functional interactions between oculomotor regions during prosaccades and antisaccades , 2005, Human brain mapping.

[3]  Chi-Hung Juan,et al.  Dissociation of spatial attention and saccade preparation. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[4]  Neil G. Muggleton,et al.  Human frontal eye fields and target switching , 2010, Cortex.

[5]  J. Gray,et al.  The psychology of fear and stress , 1971 .

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

[7]  T. Paus.  Location and function of the human frontal eye-field: A selective review , 1996, Neuropsychologia.

[8]  J. Ewert.  Advances in vertebrate neuroethology , 1982, Trends in Neurosciences.

[9]  R. Howard,et al.  Brain waves, dangerousness and deviant desires , 2002 .

[10]  Matthew F. S. Rushworth,et al.  Components of Switching Intentional Set , 2002, Journal of Cognitive Neuroscience.

[11]  Ulrich Büttner,et al.  TMS evidence for smooth pursuit gain control by the frontal eye fields. , 2009, Cerebral cortex.

[12]  Neil G. Muggleton,et al.  Modulating inhibitory control with direct current stimulation of the superior medial frontal cortex , 2011, NeuroImage.

[13]  J. Ramaekers,et al.  Acute Effects of 3,4-Methylenedioxymethamphetamine (MDMA) on Behavioral Measures of Impulsivity: Alone and in Combination with Alcohol , 2006, Neuropsychopharmacology.

[14]  Chi-Hung Juan,et al.  Human frontal eye fields and visual search. , 2003, Journal of neurophysiology.

[15]  O. Tzeng,et al.  The location probability effects of saccade reaction times are modulated in the frontal eye fields but not in the supplementary eye field. , 2011, Cerebral cortex.

[16]  G. Logan,et al.  Inhibitory Control, Impulsiveness, and Attention Deficit Hyperactivity Disorder , 2022 .

[17]  Tomás Paus,et al.  Transcranial Magnetic Stimulation of the Human Frontal Eye ®eld Facilitates Visual Awareness , 2022 .

[18]  C. Li,et al.  Performance monitoring and stop signal inhibition in abstinent patients with cocaine dependence. , 2006, Drug and alcohol dependence.

[19]  Jon Driver,et al.  Visual Selection and Posterior Parietal Cortex: Effects of Repetitive Transcranial Magnetic Stimulation on Partial Report Analyzed by Bundesen's Theory of Visual Attention , 2005, The Journal of Neuroscience.

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

[21]  Chi-Hung Juan,et al.  Predictability of saccadic behaviors is modified by transcranial magnetic stimulation over human posterior parietal cortex , 2011, Human brain mapping.

[22]  Alan Cowey,et al.  Time course of the involvement of the ventral and dorsal visual processing streams in a visuospatial task , 2007, Neuropsychologia.

[23]  Neil G. Muggleton,et al.  Control of prepotent responses by the superior medial frontal cortex , 2009, NeuroImage.

[24]  Neil G. Muggleton,et al.  Timing of Target Discrimination in Human Frontal Eye Fields , 2004, Journal of Cognitive Neuroscience.

[25]  Jeffrey D. Schall.  Frontal Eye Fields , 2009 .

[26]  Tony Ro,et al.  Inhibition of return and the human frontal eye fields , 2003, Experimental Brain Research.

[27]  Trevor W Robbins,et al.  Motor inhibition and cognitive flexibility in obsessive-compulsive disorder and trichotillomania. , 2006, The American journal of psychiatry.

[28]  O. Tzeng,et al.  Time pressure leads to inhibitory control deficits in impulsive violent offenders , 2008, Behavioural Brain Research.

[29]  Daniel C. Javitt,et al.  Activation of Inhibition: Diminishing Impulsive Behavior by Direct Current Stimulation over the Inferior Frontal Gyrus , 2011, Journal of Cognitive Neuroscience.

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

[31]  Gianluca Campana,et al.  Left frontal eye field remembers “where” but not “what” , 2007, Neuropsychologia.

[32]  Michael W. Cole,et al.  Canceling planned action: an FMRI study of countermanding saccades. , 2004, Cerebral cortex.

[33]  Shinichiro Koga,et al.  Electrocorticographic correlates of cognitive control in a stroop task—intracranial recording in epileptic patients , 2011, Human brain mapping.

[34]  Joshua W. Brown,et al.  Monitoring and Control of Action by the Frontal Lobes , 2002, Neuron.

[35]  J. Schall,et al.  Neural control of behavior: countermanding eye movements , 2000, Psychological research.

[36]  O. Tzeng,et al.  Segregation of visual selection and saccades in human frontal eye fields. , 2008, Cerebral cortex.

[37]  Alan Cowey,et al.  Temporal aspects of visual search studied by transcranial magnetic stimulation , 1997, Neuropsychologia.

[38]  Mardi J. Horowitz,et al.  The Psychology of Fear and Stress, 2nd ed , 1989 .

[39]  M. Bellgrove,et al.  Insights into the neural basis of response inhibition from cognitive and clinical neuroscience , 2009, Neuroscience & Biobehavioral Reviews.

[40]  G. Logan,et al.  Converging Evidence for a Fronto-Basal-Ganglia Network for Inhibitory Control of Action and Cognition , 2007, The Journal of Neuroscience.

[41]  Gordon D Logan,et al.  Horse-race model simulations of the stop-signal procedure. , 2003, Acta psychologica.

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

[43]  Sheng Zhang,et al.  Functional networks for cognitive control in a stop signal task: Independent component analysis , 2012, Human brain mapping.

[44]  Adam P. Morris,et al.  Executive Brake Failure following Deactivation of Human Frontal Lobe , 2006 .

[45]  Chi-Hung Juan,et al.  The timing of the involvement of the frontal eye fields and posterior parietal cortex in visual search , 2008, Neuroreport.

[46]  Rudolf Groner,et al.  Cognition and eye movements , 1982 .

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

[48]  R. Blair,et al.  The roles of orbital frontal cortex in the modulation of antisocial behavior , 2004, Brain and Cognition.

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

[50]  R. W. Schulz.  The Psychology of Fear and Stress , 1974 .

[51]  G. Logan,et al.  Impulsivity and Inhibitory Control in Normal Development and Childhood Psychopathology , 1990 .

[52]  Chi-Hung Juan,et al.  Neural correlates of impulsive-violent behavior: an event-related potential study , 2005, Neuroreport.

[53]  L. Valzelli,et al.  Reflections on experimental and human pathology of aggression , 1984, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

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

[55]  N. P. Bichot,et al.  Dissociation of visual discrimination from saccade programming in macaque frontal eye field. , 1997, Journal of neurophysiology.

[56]  Takashi R Sato,et al.  Neuronal Basis of Covert Spatial Attention in the Frontal Eye Field , 2005, The Journal of Neuroscience.

[57]  J. Rothwell,et al.  Motor and phosphene thresholds: a transcranial magnetic stimulation correlation study , 2001, Neuropsychologia.

[58]  G. Thickbroom,et al.  Transcranial magnetic stimulation of the human frontal eye field , 1996, Journal of the Neurological Sciences.