Comparing frontal eye field and superior colliculus contributions to covert spatial attention

The causal roles of the frontal eye fields (FEF) and superior colliculus (SC) in spatial selective attention have not been directly compared. Reversible inactivation is an established method for testing causality but comparing results between FEF and SC is complicated by differences in size and morphology of the two brain regions. Here we exploited the fact that inactivation of FEF and SC also changes the metrics of saccadic eye movements, providing an independent benchmark for the strength of the causal manipulation. Using monkeys trained to covertly perform a visual motion-change detection task, we found that inactivation of either FEF or SC could cause deficits in attention task performance. However, SC-induced attention deficits were found with saccade changes half the size needed to get FEF-induced attention deficits. Thus, performance in visual attention tasks is vulnerable to loss of signals from either structure, but suppression of SC activity has a more devastating effect.Superior colliculus (SC) and frontal eye fields (FEF) contain visuo-motor maps but their contributions to selective attention are not fully understood. Here, the authors perform reversible inactivations of the SC or FEF and report that loss of SC activity has a more devastating effect on attention.

[1]  D. Robinson Eye movements evoked by collicular stimulation in the alert monkey. , 1972, Vision research.

[2]  R. Wurtz,et al.  Interaction of the frontal eye field and superior colliculus for saccade generation. , 2001, Journal of neurophysiology.

[3]  T. Preuss Do Rats Have Prefrontal Cortex? The Rose-Woolsey-Akert Program Reconsidered , 1995, Journal of Cognitive Neuroscience.

[4]  Tirin Moore,et al.  Prefrontal contributions to visual selective attention. , 2013, Annual review of neuroscience.

[5]  R. Wurtz Neuronal mechanisms of visual stability , 2008, Vision Research.

[6]  W T Newsome,et al.  Target selection for saccadic eye movements: direction-selective visual responses in the superior colliculus. , 2001, Journal of neurophysiology.

[7]  John H. R. Maunsell,et al.  The effect of frontal eye field and superior colliculus lesions on saccadic latencies in the rhesus monkey. , 1987, Journal of neurophysiology.

[8]  E. Knudsen,et al.  Control from below: the role of a midbrain network in spatial attention , 2011, The European journal of neuroscience.

[9]  M. Segraves,et al.  Muscimol-induced inactivation of monkey frontal eye field: effects on visually and memory-guided saccades. , 1999, Journal of neurophysiology.

[10]  Jeffrey D Schall,et al.  The neural selection and control of saccades by the frontal eye field. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

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

[12]  J. E. Albano,et al.  Visual-motor function of the primate superior colliculus. , 1980, Annual review of neuroscience.

[13]  Jeffrey D Schall,et al.  Visuomotor Functions in the Frontal Lobe. , 2015, Annual review of vision science.

[14]  Tirin Moore,et al.  Dissociation of Response Variability from Firing Rate Effects in Frontal Eye Field Neurons during Visual Stimulation, Working Memory, and Attention , 2012, The Journal of Neuroscience.

[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]  V. Ferrera,et al.  Radial motion bias in macaque frontal eye field , 2006, Visual Neuroscience.

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

[18]  M. Huntsman,et al.  Laminar patterns of expression of GABAA receptor subunit mRNAs in monkey sensory motor cortex , 1995, The Journal of comparative neurology.

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

[20]  Jean Bullier,et al.  Spatial and temporal parameters of cortical inactivation by GABA , 1999, Journal of Neuroscience Methods.

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

[22]  Richard J Krauzlis,et al.  Changes in perceptual sensitivity related to spatial cues depends on subcortical activity , 2017, Proceedings of the National Academy of Sciences.

[23]  R. Wurtz,et al.  Superior Colliculus Cell Responses Related to Eye Movements in Awake Monkeys , 1971, Science.

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

[25]  C. Cassanello,et al.  Frontal Eye Field Neurons Signal Changes in Decision Criteria , 2009, Nature Neuroscience.

[26]  John H. Martin Autoradiographic estimation of the extent of reversible inactivation produced by microinjection of lidocaine and muscimol in the rat , 1991, Neuroscience Letters.

[27]  Tirin Moore,et al.  Changes in Visual Receptive Fields with Microstimulation of Frontal Cortex , 2006, Neuron.

[28]  James R Müller,et al.  Microstimulation of the superior colliculus focuses attention without moving the eyes. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[29]  R. Wurtz,et al.  Activity of superior colliculus in behaving monkey. II. Effect of attention on neuronal responses. , 1972, Journal of neurophysiology.

[30]  Tirin Moore,et al.  Spatial working memory alters the efficacy of input to visual cortex , 2017, Nature Communications.

[31]  E. J. Tehovnik,et al.  Eye fields in the frontal lobes of primates , 2000, Brain Research Reviews.

[32]  W T Newsome,et al.  Separate signals for target selection and movement specification in the superior colliculus. , 1999, Science.

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

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

[35]  R. Lonser,et al.  Image-guided convection-enhanced delivery of muscimol to the primate brain. , 2010, Journal of neurosurgery.

[36]  S. Akbarian,et al.  GABAA receptor subunit gene expression in human prefrontal cortex: comparison of schizophrenics and controls. , 1995, Cerebral cortex.

[37]  Ilya E. Monosov,et al.  Frontal eye field activity enhances object identification during covert visual search. , 2009, Journal of neurophysiology.

[38]  Jeffrey D. Schall,et al.  On the Evolution of the Frontal Eye Field: Comparisons of Monkeys, Apes, and Humans , 2017 .

[39]  Denis G. Pelli,et al.  ECVP '07 Abstracts , 2007, Perception.

[40]  Alexander Huk,et al.  PLDAPS: A Hardware Architecture and Software Toolbox for Neurophysiology Requiring Complex Visual Stimuli and Online Behavioral Control , 2012, Front. Neuroinform..

[41]  Laurent Madelain,et al.  Spatial deployment of attention influences both saccadic and pursuit tracking , 2005, Vision Research.

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

[43]  Steven P. Wise,et al.  Forward frontal fields: phylogeny and fundamental function , 2008, Trends in Neurosciences.

[44]  Alexandre Zénon,et al.  Attention deficits without cortical neuronal deficits , 2012, Nature.

[45]  Peter W Dicke,et al.  Neuron-specific contribution of the superior colliculus to overt and covert shifts of attention , 2004, Nature Neuroscience.

[46]  John H. R. Maunsell,et al.  Neuronal Mechanisms of Visual Attention. , 2015, Annual review of vision science.

[47]  Richard J Krauzlis,et al.  Inactivation of primate superior colliculus impairs covert selection of signals for perceptual judgments , 2010, Nature Neuroscience.

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

[49]  R. Krauzlis,et al.  Superior colliculus and visual spatial attention. , 2013, Annual review of neuroscience.

[50]  J. Duhamel,et al.  Differential effects of parietal and frontal inactivations on reaction times distributions in a visual search task , 2012, Front. Integr. Neurosci..

[51]  Yq Liu,et al.  Intention and Attention: Different functional roles for LIPd and LIPv , 2010, Nature Neuroscience.

[52]  J. L. Conway,et al.  Deficits in eye movements following frontal eye-field and superior colliculus ablations. , 1980, Journal of neurophysiology.

[53]  Richard J Krauzlis,et al.  Color-Change Detection Activity in the Primate Superior Colliculus , 2017, eNeuro.

[54]  Marc A Sommer,et al.  Circuits for presaccadic visual remapping. , 2016, Journal of neurophysiology.

[55]  Jillian H. Fecteau,et al.  Salience, relevance, and firing: a priority map for target selection , 2006, Trends in Cognitive Sciences.

[56]  Tirin Moore,et al.  A Distinct Contribution of the Frontal Eye Field to the Visual Representation of Saccadic Targets , 2014, The Journal of Neuroscience.

[57]  Richard J Krauzlis,et al.  Activity of rostral superior colliculus neurons during passive and active viewing of motion. , 2004, Journal of neurophysiology.

[58]  Anil Bollimunta,et al.  Attention as an effect not a cause , 2014, Trends in Cognitive Sciences.

[59]  M. Huntsman,et al.  Lamina-specific expression and activity-dependent regulation of seven GABAA receptor subunit mRNAs in monkey visual cortex , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[60]  N. P. Bichot,et al.  A visual salience map in the primate frontal eye field. , 2005, Progress in brain research.

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

[62]  P. May The mammalian superior colliculus: laminar structure and connections. , 2006, Progress in brain research.

[63]  Robert H. Wurtz,et al.  Subcortical Modulation of Attention Counters Change Blindness , 2004, The Journal of Neuroscience.

[64]  D H Brainard,et al.  The Psychophysics Toolbox. , 1997, Spatial vision.

[65]  T. Woolsey,et al.  A method to measure the effective spread of focally injected muscimol into the central nervous system with electrophysiology and light microscopy , 2002, Journal of Neuroscience Methods.

[66]  S. Grillner,et al.  Tectal control of locomotion, steering, and eye movements in lamprey. , 2007, Journal of neurophysiology.

[67]  Takashi R Sato,et al.  Search Efficiency but Not Response Interference Affects Visual Selection in Frontal Eye Field , 2001, Neuron.

[68]  N. J. Gandhi,et al.  Motor functions of the superior colliculus. , 2011, Annual review of neuroscience.

[69]  D G Pelli,et al.  The VideoToolbox software for visual psychophysics: transforming numbers into movies. , 1997, Spatial vision.