Deficits in saccade target selection after inactivation of superior colliculus

Saccades are rapid eye movements that orient gaze toward areas of interest in the visual scene. Neural activity correlated with saccade target selection has been identified in several brain regions, including the superior colliculus (SC), but it is not known whether the SC is directly involved in target selection, or whether the SC merely receives selection-related signals from cortex in preparation for the execution of eye movements. In monkeys, we used focal reversible inactivation to test the functional contributions of the SC to target selection during visual search, and found that inactivation resulted in clear deficits. When a target appeared in the inactivated field, saccades were often misdirected to distractor stimuli. Control tasks showed that this deficit was not caused by low-level visual or motor impairments. Our results indicate that, in addition to its well-established involvement in movement execution, the SC has an important functional role in target selection.

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

[2]  R. Wurtz,et al.  Visual receptive fields of frontal eye field neurons. , 1973, Brain research.

[3]  R. Vetter Visual localization and discrimination in squirrel monkeys with bilateral lesions of the superior colliculus. , 1975, The International journal of neuroscience.

[4]  E. Keller,et al.  Colliculoreticular organization in primate oculomotor system. , 1977, Journal of Neurophysiology.

[5]  R H Wurtz,et al.  Role of striate cortex and superior colliculus in visual guidance of saccadic eye movements in monkeys. , 1977, Journal of neurophysiology.

[6]  S Ullman,et al.  Shifts in selective visual attention: towards the underlying neural circuitry. , 1985, Human neurobiology.

[7]  R. Wurtz,et al.  Modification of saccadic eye movements by GABA-related substances. I. Effect of muscimol and bicuculline in monkey superior colliculus. , 1985, Journal of neurophysiology.

[8]  D. Sparks,et al.  The deep layers of the superior colliculus. , 1989, Reviews of oculomotor research.

[9]  D. Sparks,et al.  Population coding of the direction, amplitude, and velocity of saccadic eye movements by neurons in the superior colliculus. , 1990, Cold Spring Harbor symposia on quantitative biology.

[10]  David L. Sparks,et al.  Movement selection in advance of action in the superior colliculus , 1992, Nature.

[11]  M. Segraves,et al.  Primate frontal eye field activity during natural scanning eye movements. , 1994, Journal of neurophysiology.

[12]  J. Wolfe,et al.  Guided Search 2.0 A revised model of visual search , 1994, Psychonomic bulletin & review.

[13]  D. Sparks,et al.  Site and parameters of microstimulation: evidence for independent effects on the properties of saccades evoked from the primate superior colliculus. , 1996, Journal of neurophysiology.

[14]  H Shimazu,et al.  Monosynaptic activation of medium-lead burst neurons from the superior colliculus in the alert cat. , 1996, Journal of neurophysiology.

[15]  Michele A. Basso,et al.  Modulation of neuronal activity by target uncertainty , 1997, Nature.

[16]  P. Glimcher,et al.  Responses of intraparietal neurons to saccadic targets and visual distractors. , 1997, Journal of neurophysiology.

[17]  R. Wurtz,et al.  Reversible inactivation of monkey superior colliculus. I. Curvature of saccadic trajectory. , 1998, Journal of neurophysiology.

[18]  R. Wurtz,et al.  Reversible inactivation of monkey superior colliculus. II. Maps of saccadic deficits. , 1998, Journal of neurophysiology.

[19]  R. Walker,et al.  A model of saccade generation based on parallel processing and competitive inhibition , 1999, Behavioral and Brain Sciences.

[20]  Stephen G Lomber,et al.  The advantages and limitations of permanent or reversible deactivation techniques in the assessment of neural function , 1999, Journal of Neuroscience Methods.

[21]  James J. Clark Spatial attention and latencies of saccadic eye movements , 1999, Vision Research.

[22]  M. Shadlen,et al.  Neural correlates of a decision in the dorsolateral prefrontal cortex of the macaque , 1999, Nature Neuroscience.

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

[24]  P. H. Schiller,et al.  Express averaging saccades in monkeys , 1999, Vision Research.

[25]  Peter H Schiller,et al.  The effects of anterior arcuate and dorsomedial frontal cortex lesions on visually guided eye movements: 2. Paired and multiple targets , 2000, Vision Research.

[26]  R. Kass,et al.  Neuronal activity in macaque supplementary eye field during planning of saccades in response to pattern and spatial cues. , 2000, Journal of neurophysiology.

[27]  A. Mikami,et al.  Search target selection in monkey prefrontal cortex. , 2000, Journal of neurophysiology.

[28]  C. Koch,et al.  A saliency-based search mechanism for overt and covert shifts of visual attention , 2000, Vision Research.

[29]  W. Newsome,et al.  Neural basis of a perceptual decision in the parietal cortex (area LIP) of the rhesus monkey. , 2001, Journal of neurophysiology.

[30]  D. Sparks,et al.  A simple method for constructing microinjectrodes for reversible inactivation in behaving monkeys , 2001, Journal of Neuroscience Methods.

[31]  M. Goldberg,et al.  The Role of the Lateral Intraparietal Area of the Monkey in the Generation of Saccades and Visuospatial Attention , 2002, Annals of the New York Academy of Sciences.

[32]  R. Krauzlis,et al.  Neural Correlates of Target Choice for Pursuit and Saccades in the Primate Superior Colliculus , 2002, Neuron.

[33]  J. Duhamel,et al.  Saccadic Target Selection Deficits after Lateral Intraparietal Area Inactivation in Monkeys , 2002, The Journal of Neuroscience.

[34]  E. Keller,et al.  Saccade target selection in the superior colliculus during a visual search task. , 2002, Journal of neurophysiology.

[35]  Michiyo Iba,et al.  Involvement of the dorsolateral prefrontal cortex of monkeys in visuospatial target selection. , 2003, Journal of neurophysiology.

[36]  R. Wurtz,et al.  Sequential activity of simultaneously recorded neurons in the superior colliculus during curved saccades. , 2003, Journal of neurophysiology.

[37]  Peter H Schiller,et al.  Cortical inhibitory circuits in eye‐movement generation , 2003, The European journal of neuroscience.

[38]  Robert M McPeek,et al.  Competition between saccade goals in the superior colliculus produces saccade curvature. , 2003, Journal of neurophysiology.

[39]  F. P. Ottes,et al.  Collicular involvement in a saccadic colour discrimination task , 2004, Experimental Brain Research.

[40]  P Pasik,et al.  Extrageniculostriate vision in the monkey , 1981, Experimental Brain Research.

[41]  J. Rovamo,et al.  An estimation and application of the human cortical magnification factor , 2004, Experimental Brain Research.

[42]  O. Hikosaka,et al.  Minimal synaptic delay in the saccadic output pathway of the superior colliculus studied in awake monkey , 1996, Experimental Brain Research.

[43]  R. Wurtz,et al.  Saccadic eye movements following injection of lidocaine into the superior colliculus , 2004, Experimental Brain Research.

[44]  S. Snyder,et al.  Separate Signals for Target Selection and Movement Specification in the Superior Colliculus , 2022 .