Neurons in the lateral intraparietal area create a priority map by the combination of disparate signals

Primates search for objects in the visual field with eye movements. We recorded the activity of neurons in the lateral intraparietal area (LIP) in animals performing a visual search task in which they were free to move their eyes, and reported the results of the search with a hand movement. We distinguished three independent signals: (1) a visual signal describing the abrupt onset of a visual stimulus in the receptive field; (2) a saccadic signal predicting the monkey’s saccadic reaction time independently of the nature of the stimulus; (3) a cognitive signal distinguishing between the search target and a distractor independently of the direction of the impending saccade. The cognitive signal became significant on average 27 ms after the saccadic signal but before the saccade was made. The three signals summed in a manner discernable at the level of the single neuron.

[1]  J Metcalfe Novelty monitoring, metacognition, and control in a composite holographic associative recall model: implications for Korsakoff amnesia. , 1993, Psychological review.

[2]  D. McCormick,et al.  Enhancement of visual responsiveness by spontaneous local network activity in vivo. , 2007, Journal of neurophysiology.

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

[4]  M. Goldberg,et al.  Response of neurons in the lateral intraparietal area to a distractor flashed during the delay period of a memory-guided saccade. , 2000, Journal of neurophysiology.

[5]  Leslie G. Ungerleider,et al.  Cortical connections of inferior temporal area TEO in macaque monkeys , 1993, The Journal of comparative neurology.

[6]  Leslie G. Ungerleider,et al.  Organization of visual inputs to the inferior temporal and posterior parietal cortex in macaques , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[7]  Jacqueline Gottlieb,et al.  LIP responses to a popout stimulus are reduced if it is overtly ignored , 2006, Nature Neuroscience.

[8]  A. Leventhal,et al.  Signal timing across the macaque visual system. , 1998, Journal of neurophysiology.

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

[10]  J. Assad,et al.  Dissociation of visual, motor and predictive signals in parietal cortex during visual guidance , 1999, Nature Neuroscience.

[11]  J. Duhamel,et al.  Multisensory Integration in the Ventral Intraparietal Area of the Macaque Monkey , 2007, The Journal of Neuroscience.

[12]  D. V. van Essen,et al.  Corticocortical connections of visual, sensorimotor, and multimodal processing areas in the parietal lobe of the macaque monkey , 2000, The Journal of comparative neurology.

[13]  Jeffrey D. Schall,et al.  Effect of target-distractor similarity on FEF visual selection in the absence of the target , 2003, Experimental Brain Research.

[14]  R. Wurtz,et al.  Visual and oculomotor functions of monkey substantia nigra pars reticulata. III. Memory-contingent visual and saccade responses. , 1983, Journal of neurophysiology.

[15]  Joseph J. Paton,et al.  The primate amygdala represents the positive and negative value of visual stimuli during learning , 2006, Nature.

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

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

[18]  L H Snyder,et al.  Nonspatial saccade-specific activation in area LIP of monkey parietal cortex. , 2003, Journal of neurophysiology.

[19]  N. P. Bichot,et al.  Perceptual and motor processing stages identified in the activity of macaque frontal eye field neurons during visual search. , 1996, Journal of neurophysiology.

[20]  M. Goldberg,et al.  The time course of perisaccadic receptive field shifts in the lateral intraparietal area of the monkey. , 2003, Journal of neurophysiology.

[21]  Michael N. Shadlen,et al.  Probabilistic reasoning by neurons , 2007, Nature.

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

[23]  S. Yantis,et al.  Selective visual attention and perceptual coherence , 2006, Trends in Cognitive Sciences.

[24]  Lance M. Optican,et al.  Unix-based multiple-process system, for real-time data acquisition and control , 1982 .

[25]  M. Goldberg,et al.  The representation of visual salience in monkey parietal cortex , 1998, Nature.

[26]  M. Paré,et al.  Neuronal activity in superior colliculus signals both stimulus identity and saccade goals during visual conjunction search. , 2007, Journal of vision.

[27]  H. Spitzer,et al.  Temporal encoding of two-dimensional patterns by single units in primate inferior temporal cortex. I. Response characteristics. , 1987, Journal of neurophysiology.

[28]  Michael L. Platt,et al.  Neural correlates of decision variables in parietal cortex , 1999, Nature.

[29]  A. Treisman,et al.  A feature-integration theory of attention , 1980, Cognitive Psychology.

[30]  J. Movshon,et al.  The Timing of Response Onset and Offset in Macaque Visual Neurons , 2002, The Journal of Neuroscience.

[31]  B. C. Motter,et al.  The guidance of eye movements during active visual search , 1998, Vision Research.

[32]  R. Yuste,et al.  Linear Summation of Excitatory Inputs by CA1 Pyramidal Neurons , 1999, Neuron.

[33]  J. Maunsell,et al.  Neuronal correlates of inferred motion in primate posterior parietal cortex , 1995, Nature.

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

[35]  M. Paré,et al.  Temporal processing of saccade targets in parietal cortex area LIP during visual search. , 2007, Journal of neurophysiology.

[36]  D. Ferster,et al.  Linearity of summation of synaptic potentials underlying direction selectivity in simple cells of the cat visual cortex. , 1993, Science.

[37]  R. Andersen,et al.  Saccade-related activity in the lateral intraparietal area. I. Temporal properties; comparison with area 7a. , 1991, Journal of neurophysiology.

[38]  James W Bisley,et al.  Neural correlates of attention and distractibility in the lateral intraparietal area. , 2006, Journal of neurophysiology.

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

[40]  Puiu F. Balan,et al.  Integration of Visuospatial and Effector Information during Symbolically Cued Limb Movements in Monkey Lateral Intraparietal Area , 2006, The Journal of Neuroscience.

[41]  David J. Freedman,et al.  Experience-dependent representation of visual categories in parietal cortex , 2006, Nature.

[42]  J R Duhamel,et al.  The updating of the representation of visual space in parietal cortex by intended eye movements. , 1992, Science.

[43]  M. Goldberg,et al.  Activity in the Lateral Intraparietal Area Predicts the Goal and Latency of Saccades in a Free-Viewing Visual Search Task , 2006, The Journal of Neuroscience.

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

[45]  John H. R. Maunsell,et al.  Shape selectivity in primate lateral intraparietal cortex , 1998, Nature.

[46]  R. Andersen,et al.  Visual receptive field organization and cortico‐cortical connections of the lateral intraparietal area (area LIP) in the macaque , 1990, The Journal of comparative neurology.

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

[48]  M. Goldberg,et al.  A Rapid and Precise On-Response in Posterior Parietal Cortex , 2004, The Journal of Neuroscience.