Influence of history on saccade countermanding performance in humans and macaque monkeys

The stop-signal or countermanding task probes the ability to control action by requiring subjects to withhold a planned movement in response to an infrequent stop signal which they do with variable success depending on the delay of the stop signal. We investigated whether performance of humans and macaque monkeys in a saccade countermanding task was influenced by stimulus and performance history. In spite of idiosyncrasies across subjects several trends were evident in both humans and monkeys. Response time decreased after successive trials with no stop signal. Response time increased after successive trials with a stop signal. However, post-error slowing was not observed. Increased response time was observed mainly or only after cancelled (signal inhibit) trials and not after noncancelled (signal respond) trials. These global trends were based on rapid adjustments of response time in response to momentary fluctuations in the fraction of stop signal trials. The effects of trial sequence on the probability of responding were weaker and more idiosyncratic across subjects when stop signal fraction was fixed. However, both response time and probability of responding were influenced strongly by variations in the fraction of stop signal trials. These results indicate that the race model of countermanding performance requires extension to account for these sequential dependencies and provide a basis for physiological studies of executive control of countermanding saccade performance.

[1]  J. Schall,et al.  Performance monitoring by the supplementary eye ® eld , 2000 .

[2]  D P Munoz,et al.  On your mark, get set: brainstem circuitry underlying saccadic initiation. , 2000, Canadian journal of physiology and pharmacology.

[3]  P M Rabbitt,et al.  Error-Detection and Correction Latencies as a Function of S-R Compatibility , 1967, The Quarterly journal of experimental psychology.

[4]  C. Eriksen,et al.  Use of a delayed signal to stop a visual reaction-time response. , 1966 .

[5]  B. Bergum,et al.  Attention and performance IX , 1982 .

[6]  Leanne Boucher,et al.  Stopping eye and hand movements: Are the processes independent? , 2007, Perception & psychophysics.

[7]  D. Munoz,et al.  Neuronal Activity in Monkey Superior Colliculus Related to the Initiation of Saccadic Eye Movements , 1997, The Journal of Neuroscience.

[8]  D. B. Preston The Analysis of Time Series: Theory and Practice , 1977 .

[9]  R. D. Gordon,et al.  Executive control of visual attention in dual-task situations. , 2001, Psychological review.

[10]  Vision Research , 1961, Nature.

[11]  D Laming,et al.  Autocorrelation of choice-reaction times. , 1979, Acta psychologica.

[12]  D. Meyer,et al.  Attention and Performance XIV , 1973 .

[13]  T. Carr,et al.  Inhibitory Processes in Attention, Memory and Language , 1994 .

[14]  M. W. van der Molen,et al.  The duration of response inhibition in the stop-signal paradigm varies with response force. , 2003, Acta psychologica.

[15]  D P Munoz,et al.  Role of Primate Superior Colliculus in Preparation and Execution of Anti-Saccades and Pro-Saccades , 1999, The Journal of Neuroscience.

[16]  Gordon D Logan,et al.  Evidence for an Error Monitoring Deficit in Attention Deficit Hyperactivity Disorder , 2004, Journal of abnormal child psychology.

[17]  D. Munoz,et al.  Saccadic Probability Influences Motor Preparation Signals and Time to Saccadic Initiation , 1998, The Journal of Neuroscience.

[18]  G. Logan,et al.  An interactive race model of countermanding saccades , 2003 .

[19]  Martina Rieger,et al.  Inhibitory after‐effects in the stop signal paradigm , 1999 .

[20]  D. Norman,et al.  Attention to Action: Willed and Automatic Control of Behavior Technical Report No. 8006. , 1980 .

[21]  A. Baddeley,et al.  Working memory and executive control. , 1996, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

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

[23]  R. Carpenter,et al.  Saccadic countermanding: a comparison of central and peripheral stop signals , 2001, Vision Research.

[24]  M. Botvinick,et al.  Conflict monitoring and cognitive control. , 2001, Psychological review.

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

[26]  N. P. Bichot,et al.  Effects of similarity and history on neural mechanisms of visual selection , 1999, Nature Neuroscience.

[27]  J. Schall On building a bridge between brain and behavior. , 2004, Annual review of psychology.

[28]  D. Alan Allport,et al.  SHIFTING INTENTIONAL SET - EXPLORING THE DYNAMIC CONTROL OF TASKS , 1994 .

[29]  D. Tucker,et al.  Medial Frontal Cortex in Action Monitoring , 2000, The Journal of Neuroscience.

[30]  Veit Stuphorn,et al.  Neuronal control and monitoring of initiation of movements , 2002, Muscle & nerve.

[31]  Jillian H. Fecteau,et al.  Exploring the consequences of the previous trial , 2003, Nature Reviews Neuroscience.

[32]  Daniel H. Mathalon,et al.  Fore-period effect and stop-signal reaction time , 2005, Experimental Brain Research.

[33]  C. Carter,et al.  The Timing of Action-Monitoring Processes in the Anterior Cingulate Cortex , 2002, Journal of Cognitive Neuroscience.

[34]  J. Schall,et al.  Neural selection and control of visually guided eye movements. , 1999, Annual review of neuroscience.

[35]  J. Schall,et al.  Executive control of countermanding saccades by the supplementary eye field , 2006, Nature Neuroscience.

[36]  A. Dobson An introduction to generalized linear models , 1990 .

[37]  K. R. Ridderinkhof,et al.  The Role of the Medial Frontal Cortex in Cognitive Control , 2004, Science.

[38]  D P Munoz,et al.  Influence of previous visual stimulus or saccade on saccadic reaction times in monkey. , 1999, Journal of neurophysiology.

[39]  Tracy L. Taylor,et al.  The Interplay of Stop Signal Inhibition and Inhibition of Return , 2003, The Quarterly journal of experimental psychology. A, Human experimental psychology.

[40]  Clay B. Holroyd,et al.  Reinforcement-related brain potentials from medial frontal cortex: origins and functional significance , 2004, Neuroscience & Biobehavioral Reviews.

[41]  D. Norman,et al.  Attention to action: Willed and automatic control , 1980 .

[42]  Gordon D. Logan,et al.  Dependence and Independence in Responding to Double Stimulation : A Comparison of Stop , Change , and Dual-Task Paradigms , 1986 .

[43]  M. Goldberg,et al.  Neurons in monkey prefrontal cortex that track past or predict future performance. , 2000, Science.

[44]  A. Baddeley,et al.  The multi-component model of working memory: Explorations in experimental cognitive psychology , 2006, Neuroscience.

[45]  R. Carpenter,et al.  The influence of urgency on decision time , 2000, Nature Neuroscience.

[46]  James L. McClelland,et al.  On the control of automatic processes: a parallel distributed processing account of the Stroop effect. , 1990, Psychological review.

[47]  D P Munoz,et al.  Neuronal Correlates for Preparatory Set Associated with Pro-Saccades and Anti-Saccades in the Primate Frontal Eye Field , 2000, The Journal of Neuroscience.

[48]  P. M. A. RABBITT,et al.  Error Correction Time without External Error Signals , 1966, Nature.

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

[50]  W. Newsome,et al.  Matching Behavior and the Representation of Value in the Parietal Cortex , 2004, Science.

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

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

[53]  D. Munoz,et al.  t Immediate Neural Plasticity Shapes Motor Performance , 2000, The Journal of Neuroscience.

[54]  G. Logan Executive control of thought and action , 1985 .

[55]  D P Munoz,et al.  Saccadic reaction time in the monkey: advanced preparation of oculomotor programs is primarily responsible for express saccade occurrence. , 1996, Journal of neurophysiology.

[56]  Richard J Krauzlis,et al.  Cancelling of pursuit and saccadic eye movements in humans and monkeys. , 2003, Journal of neurophysiology.

[57]  A. Vandierendonck,et al.  Inhibiting responses when switching: Does it matter? , 2005, Experimental psychology.

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

[59]  G. Logan,et al.  On the ability to inhibit simple and choice reaction time responses: a model and a method. , 1984, Journal of experimental psychology. Human perception and performance.

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

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

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

[63]  Jonathan D. Cohen,et al.  Mechanisms underlying dependencies of performance on stimulus history in a two-alternative forced-choice task , 2002, Cognitive, affective & behavioral neuroscience.

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

[65]  M. C. Borja,et al.  An Introduction to Generalized Linear Models , 2009 .

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

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

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

[69]  Joshua W. Brown,et al.  Performance Monitoring by the Anterior Cingulate Cortex During Saccade Countermanding , 2003, Science.

[70]  E. Procyk,et al.  The effects of sequence structure and reward schedule on serial reaction time learning in the monkey. , 2000, Brain research. Cognitive brain research.

[71]  W. Wolf,et al.  Occurrence of human express saccades depends on stimulus uncertainty and stimulus sequence , 2004, Experimental Brain Research.

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

[73]  D. Sparks Functional properties of neurons in the monkey superior colliculus: Coupling of neuronal activity and saccade onset , 1978, Brain Research.

[74]  M. Moscovitch,et al.  Attention and Performance 15: Conscious and Nonconscious Information Processing , 1994 .

[75]  P. Rabbitt Errors and error correction in choice-response tasks. , 1966, Journal of experimental psychology.

[76]  EEG measures of executive function , 1998 .

[77]  K. R. Ridderinkhof,et al.  Effects of stop-signal probability in the stop-signal paradigm: The N2/P3 complex further validated , 2004, Brain and Cognition.

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

[79]  R. H. S. Carpenter,et al.  Neural computation of log likelihood in control of saccadic eye movements , 1995, Nature.

[80]  Bryan Rodgers,et al.  What does a Man do after he Makes an Error? An Analysis of Response Programming , 1977 .

[81]  A. Vandierendonck,et al.  The interaction between stop signal inhibition and distractor interference in the flanker and Stroop task. , 2004, Acta psychologica.

[82]  Pierpaolo Pani,et al.  Inhibitory control of reaching movements in humans , 2009, Experimental Brain Research.