Spike-field activity in parietal area LIP during coordinated reach and saccade movements

The posterior parietal cortex is situated between visual and motor areas and supports coordinated visually guided behavior. Area LIP in the intraparietal sulcus contains representations of visual space and has been extensively studied in the context of saccades. However, area LIP has not been studied during coordinated movements, so it is not known whether saccadic representations in area LIP are influenced by coordinated behavior. Here, we studied spiking and local field potential (LFP) activity in area LIP while subjects performed coordinated reaches and saccades or saccades alone to remembered target locations to test whether activity in area LIP is influenced by the presence of a coordinated reach. We find that coordination significantly changes the activity of individual neurons in area LIP, increasing or decreasing the firing rate when a reach is made with a saccade compared with when a saccade is made alone. Analyzing spike-field coherence demonstrates that area LIP neurons whose firing rate is suppressed during the coordinated task have activity temporally correlated with nearby LFP activity, which reflects the synaptic activity of populations of neurons. Area LIP neurons whose firing rate increases during the coordinated task do not show significant spike-field coherence. Furthermore, LFP power in area LIP is suppressed and does not increase when a coordinated reach is made with a saccade. These results demonstrate that area LIP neurons display different responses to coordinated reach and saccade movements, and that different spike rate responses are associated with different patterns of correlated activity. The population of neurons whose firing rate is suppressed is coherently active with local populations of LIP neurons. Overall, these results suggest that area LIP plays a role in coordinating visually guided actions through suppression of coherent patterns of saccade-related activity.

[1]  Bijan Pesaran,et al.  Temporal structure in neuronal activity during working memory in macaque parietal cortex , 2000, Nature Neuroscience.

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

[3]  Christophe Jouffrais,et al.  Neuronal activity related to eye-hand coordination in the primate premotor cortex , 1999, Experimental Brain Research.

[4]  C. Prablanc,et al.  Automatic control during hand reaching at undetected two-dimensional target displacements. , 1992, Journal of neurophysiology.

[5]  H. Seo,et al.  Lateral Intraparietal Cortex and Reinforcement Learning during a Mixed-Strategy Game , 2009, The Journal of Neuroscience.

[6]  J D Crawford,et al.  Proprioceptive guidance of saccades in eye-hand coordination. , 2006, Journal of neurophysiology.

[7]  P. Goldman-Rakic,et al.  Posterior parietal cortex in rhesus monkey: I. Parcellation of areas based on distinctive limbic and sensory corticocortical connections , 1989, The Journal of comparative neurology.

[8]  Christopher C. Pack,et al.  Pattern Motion Selectivity of Spiking Outputs and Local Field Potentials in Macaque Visual Cortex , 2009, The Journal of Neuroscience.

[9]  E. M. Rouiller,et al.  Thalamocortical and the dual pattern of corticothalamic projections of the posterior parietal cortex in macaque monkeys , 2007, Neuroscience.

[10]  J. Alonso,et al.  Lateral-posterior and pulvinar reaching cells—comparison with parietal area 5a: a study in behaving Macaca nemestrina monkeys , 2004, Experimental Brain Research.

[11]  B. Dosher,et al.  The role of attention in the programming of saccades , 1995, Vision Research.

[12]  J. Donoghue,et al.  Neural discharge and local field potential oscillations in primate motor cortex during voluntary movements. , 1998, Journal of neurophysiology.

[13]  B. Troost,et al.  Comparative velocities of different types of fast eye movements in man. , 1975, Investigative ophthalmology.

[14]  Pascal Fries,et al.  Neuronal Synchronization in Human Posterior Parietal Cortex during Reach Planning , 2010, The Journal of Neuroscience.

[15]  A. Fuchs,et al.  Further properties of the human saccadic system: eye movements and correction saccades with and without visual fixation points. , 1969, Vision research.

[16]  Roger D. Traub,et al.  Simulation of Gamma Rhythms in Networks of Interneurons and Pyramidal Cells , 1997, Journal of Computational Neuroscience.

[17]  J. Tigges,et al.  Cross-Correlation Analysis of Electroencephalographic Potentials and Slow Membrane Transients , 1965, Science.

[18]  K. Hoffmann,et al.  A possible role of the superior colliculus in eye-hand coordination. , 2001, Progress in brain research.

[19]  E. Fetz,et al.  Coherent 25- to 35-Hz oscillations in the sensorimotor cortex of awake behaving monkeys. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[20]  Y. Rossetti,et al.  Optic ataxia and the function of the dorsal stream: Contributions to perception and action , 2009, Neuropsychologia.

[21]  M. Posner,et al.  Processing of visual feedback in rapid movements. , 1968, Journal of experimental psychology.

[22]  Zygmunt Pizlo,et al.  Effect of Freeing the Head on Eye Movement Characteristics during Three-Dimensional Shifts of Gaze and Tracking , 2012 .

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

[24]  Driss Boussaoud,et al.  Hand modulation of visual, preparatory, and saccadic activity in the monkey frontal eye field. , 2011, Cerebral cortex.

[25]  A. Pouget,et al.  Variance as a Signature of Neural Computations during Decision Making , 2011, Neuron.

[26]  J. Gold,et al.  The neural basis of decision making. , 2007, Annual review of neuroscience.

[27]  Byron M. Yu,et al.  Reference frames for reach planning in macaque dorsal premotor cortex. , 2007, Journal of neurophysiology.

[28]  Bijan Pesaran,et al.  Free choice activates a decision circuit between frontal and parietal cortex , 2008, Nature.

[29]  Thrishantha Nanayakkara,et al.  Saccade adaptation in response to altered arm dynamics. , 2003, Journal of neurophysiology.

[30]  K. Hoffmann,et al.  Influence of arm movements on saccades in humans , 2000, The European journal of neuroscience.

[31]  Michael Okun,et al.  The Subthreshold Relation between Cortical Local Field Potential and Neuronal Firing Unveiled by Intracellular Recordings in Awake Rats , 2010, The Journal of Neuroscience.

[32]  A. Pérez-Villalba Rhythms of the Brain, G. Buzsáki. Oxford University Press, Madison Avenue, New York (2006), Price: GB £42.00, p. 448, ISBN: 0-19-530106-4 , 2008 .

[33]  H. Bekkering,et al.  Ocular gaze is anchored to the target of an ongoing pointing movement. , 2000, Journal of neurophysiology.

[34]  R Caminiti,et al.  Early coding of visuomanual coordination during reaching in parietal area PEc. , 2001, Journal of neurophysiology.

[35]  L. Stark,et al.  The main sequence, a tool for studying human eye movements , 1975 .

[36]  N. Logothetis,et al.  Very slow activity fluctuations in monkey visual cortex: implications for functional brain imaging. , 2003, Cerebral cortex.

[37]  R. Shapley,et al.  Spatial Spread of the Local Field Potential and its Laminar Variation in Visual Cortex , 2009, The Journal of Neuroscience.

[38]  M. Carandini,et al.  Stimulus contrast modulates functional connectivity in visual cortex , 2009, Nature Neuroscience.

[39]  H. Bekkering,et al.  Gaze anchoring to a pointing target is present during the entire pointing movement and is driven by a non-visual signal. , 2001, Journal of neurophysiology.

[40]  Eun Jung Hwang,et al.  Effects of visual stimulation on LFPs, spikes, and LFP-spike relations in PRR. , 2011, Journal of neurophysiology.

[41]  M. Shadlen,et al.  Response of Neurons in the Lateral Intraparietal Area during a Combined Visual Discrimination Reaction Time Task , 2002, The Journal of Neuroscience.

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

[43]  R. Andersen,et al.  Intentional maps in posterior parietal cortex. , 2002, Annual review of neuroscience.

[44]  Christopher A. Buneo,et al.  Direct visuomotor transformations for reaching , 2002, Nature.

[45]  M. Carandini,et al.  Local Origin of Field Potentials in Visual Cortex , 2009, Neuron.

[46]  R. Andersen,et al.  The thalamic relations of the caudal inferior parietal lobule and the lateral prefrontal cortex in monkeys: Divergent cortical projections from cell clusters in the medial pulvinar nucleus , 1985, The Journal of comparative neurology.

[47]  M. A. Smith,et al.  Stimulus Selectivity and Spatial Coherence of Gamma Components of the Local Field Potential , 2011, The Journal of Neuroscience.

[48]  W. Werner,et al.  Neurons in the Primate Superior Colliculus are Active Before and During Arm Movements to Visual Targets , 1993, The European journal of neuroscience.

[49]  J D Crawford,et al.  Spatial transformations for eye-hand coordination. , 2004, Journal of neurophysiology.

[50]  P. Glimcher,et al.  Reward Value-Based Gain Control: Divisive Normalization in Parietal Cortex , 2011, The Journal of Neuroscience.

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

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

[53]  M. Hayhoe,et al.  In what ways do eye movements contribute to everyday activities? , 2001, Vision Research.

[54]  M. Shadlen,et al.  Representation of Confidence Associated with a Decision by Neurons in the Parietal Cortex , 2009, Science.

[55]  R. Andersen,et al.  Dorsal Premotor Neurons Encode the Relative Position of the Hand, Eye, and Goal during Reach Planning , 2006, Neuron.

[56]  P. Fries Neuronal gamma-band synchronization as a fundamental process in cortical computation. , 2009, Annual review of neuroscience.

[57]  W. Helsen,et al.  Coupling of Eye, Finger, Elbow, and Shoulder Movements During Manual Aiming , 2000, Journal of motor behavior.

[58]  J. Csicsvari,et al.  Organization of cell assemblies in the hippocampus , 2003, Nature.

[59]  U. Mitzdorf Current source-density method and application in cat cerebral cortex: investigation of evoked potentials and EEG phenomena. , 1985, Physiological reviews.

[60]  R. Desimone,et al.  Modulation of Oscillatory Neuronal Synchronization by Selective Visual Attention , 2001, Science.

[61]  Kenway Louie,et al.  Separating Value from Choice: Delay Discounting Activity in the Lateral Intraparietal Area , 2010, The Journal of Neuroscience.

[62]  J. V. Gisbergen,et al.  A parametric analysis of human saccades in different experimental paradigms , 1987, Vision Research.

[63]  J. Bisley,et al.  A pure salience response in posterior parietal cortex. , 2011, Cerebral cortex.

[64]  M. Mascaro,et al.  Temporal evolution and strength of neural activity in parietal cortex during eye and hand movements. , 2007, Cerebral cortex.

[65]  K. Hoffmann,et al.  Role of the rostral superior colliculus in gaze anchoring during reach movements. , 2010, Journal of neurophysiology.

[66]  Bijan Pesaran Neural correlations, decisions, and actions , 2010, Current Opinion in Neurobiology.

[67]  H. Deubel,et al.  Attentional landscapes in reaching and grasping , 2010, Vision Research.

[68]  Janita Turchi,et al.  Pulvinar Inactivation Disrupts Selection of Movement Plans , 2010, The Journal of Neuroscience.

[69]  M. Scanziani,et al.  Instantaneous Modulation of Gamma Oscillation Frequency by Balancing Excitation with Inhibition , 2009, Neuron.

[70]  Partha P. Mitra,et al.  Sampling Properties of the Spectrum and Coherency of Sequences of Action Potentials , 2000, Neural Computation.

[71]  R. Andersen,et al.  Cortical Local Field Potential Encodes Movement Intentions in the Posterior Parietal Cortex , 2005, Neuron.

[72]  R. M. Siegel,et al.  Encoding of spatial location by posterior parietal neurons. , 1985, Science.

[73]  R. Andersen,et al.  Saccade-related activity in the lateral intraparietal area. II. Spatial properties. , 1991, Journal of neurophysiology.

[74]  Christophe Bourdin,et al.  Role of sensory information in updating internal models of the effector during arm tracking. , 2003, Progress in brain research.

[75]  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.

[76]  Francisco Gonzalez,et al.  Sensorimotor unit activity related to intention in the Pulvinar of behaving Cebus Apella monkeys , 2004, Experimental Brain Research.

[77]  Roger D. Traub,et al.  Rhythm Generation through Period Concatenation in Rat Somatosensory Cortex , 2008, PLoS Comput. Biol..

[78]  Valentin Dragoi,et al.  Adaptive Changes in Neuronal Synchronization in Macaque V4 , 2011, The Journal of Neuroscience.

[79]  M. Goodale,et al.  Visual control of reaching movements without vision of the limb , 1986, Experimental Brain Research.

[80]  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.

[81]  H. Deubel,et al.  Independent Allocation of Attention to Eye and Hand Targets in Coordinated Eye-Hand Movements , 2011, Psychological science.

[82]  E. Fetz,et al.  Oscillatory activity in sensorimotor cortex of awake monkeys: synchronization of local field potentials and relation to behavior. , 1996, Journal of neurophysiology.

[83]  Jun Tanji,et al.  Distribution of eye- and arm-movement-related neuronal activity in the SEF and in the SMA and Pre-SMA of monkeys. , 2002, Journal of neurophysiology.

[84]  R Caminiti,et al.  Eye-hand coordination during reaching. II. An analysis of the relationships between visuomanual signals in parietal cortex and parieto-frontal association projections. , 2001, Cerebral cortex.

[85]  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.

[86]  Bijan Pesaran,et al.  A Relative Position Code for Saccades in Dorsal Premotor Cortex , 2010, The Journal of Neuroscience.

[87]  R. M. Siegel,et al.  Corticocortical connections of anatomically and physiologically defined subdivisions within the inferior parietal lobule , 1990, The Journal of comparative neurology.

[88]  R. Desimone,et al.  High-Frequency, Long-Range Coupling Between Prefrontal and Visual Cortex During Attention , 2009, Science.

[89]  Jacqueline Gottlieb,et al.  Functional Significance of Nonspatial Information in Monkey Lateral Intraparietal Area , 2009, The Journal of Neuroscience.

[90]  Bijan Pesaran,et al.  Reaction Time Correlations during Eye–Hand Coordination: Behavior and Modeling , 2011, The Journal of Neuroscience.

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

[92]  Adrián Ponce-Alvarez,et al.  Context-related frequency modulations of macaque motor cortical LFP beta oscillations. , 2012, Cerebral cortex.

[93]  N Kopell,et al.  Neuronal assembly dynamics in the beta1 frequency range permits short-term memory , 2011, Proceedings of the National Academy of Sciences.

[94]  Anthony R. Dickinson,et al.  Eye-hand coordination: saccades are faster when accompanied by a coordinated arm movement. , 2002, Journal of neurophysiology.

[95]  Stuart N Baker,et al.  Synchronization in monkey motor cortex during a precision grip task. II. effect of oscillatory activity on corticospinal output. , 2003, Journal of neurophysiology.

[96]  Xiao-Jing Wang,et al.  What determines the frequency of fast network oscillations with irregular neural discharges? I. Synaptic dynamics and excitation-inhibition balance. , 2003, Journal of neurophysiology.

[97]  E. Miller,et al.  Top-Down Versus Bottom-Up Control of Attention in the Prefrontal and Posterior Parietal Cortices , 2007, Science.

[98]  C. Colby,et al.  Spatial updating in area LIP is independent of saccade direction. , 2006, Journal of neurophysiology.

[99]  J Tanji,et al.  Visually guided saccade versus eye-hand reach: contrasting neuronal activity in the cortical supplementary and frontal eye fields. , 1996, Journal of neurophysiology.

[100]  R. Andersen,et al.  Memory related motor planning activity in posterior parietal cortex of macaque , 1988, Experimental Brain Research.

[101]  F Bremmer,et al.  Eye position effects on the neuronal activity of dorsal premotor cortex in the macaque monkey. , 1998, Journal of neurophysiology.

[102]  H. Deubel,et al.  Delayed Saccades, but Not Delayed Manual Aiming Movements, Require Visual Attention Shifts , 2003, Annals of the New York Academy of Sciences.

[103]  M. Jeannerod,et al.  Optimal response of eye and hand motor systems in pointing at a visual target , 1979, Biological Cybernetics.

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

[105]  Valentin Dragoi,et al.  Adaptation-induced synchronization in laminar cortical circuits , 2011, Proceedings of the National Academy of Sciences.

[106]  Alexander Kraskov,et al.  Selectivity for Grasp in Local Field Potential and Single Neuron Activity Recorded Simultaneously from M1 and F5 in the Awake Macaque Monkey , 2008, The Journal of Neuroscience.

[107]  P. Glimcher,et al.  Activity in Posterior Parietal Cortex Is Correlated with the Relative Subjective Desirability of Action , 2004, Neuron.

[108]  Michael J. Shelley,et al.  LFP spectral peaks in V1 cortex: network resonance and cortico-cortical feedback , 2010, Journal of Computational Neuroscience.

[109]  Lamarre,et al.  Self-moved target eye tracking in control and deafferented subjects: roles of arm motor command and proprioception in arm-eye coordination. , 1996, Journal of neurophysiology.

[110]  R. Johansson,et al.  Eye–Hand Coordination in Object Manipulation , 2001, The Journal of Neuroscience.

[111]  D. Carey,et al.  Neuropsychological perspectives on eye-hand coordination in visually-guided reaching. , 2002, Progress in brain research.

[112]  P. Mitra,et al.  Analysis of dynamic brain imaging data. , 1998, Biophysical journal.

[113]  Theodoros P. Zanos,et al.  Removal of spurious correlations between spikes and local field potentials. , 2011, Journal of neurophysiology.

[114]  H. Barbas,et al.  Diversity of laminar connections linking periarcuate and lateral intraparietal areas depends on cortical structure , 2006, The European journal of neuroscience.

[115]  Jacqueline Gottlieb,et al.  Spatial and non-spatial functions of the parietal cortex , 2010, Current Opinion in Neurobiology.

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

[117]  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.

[118]  Pascal Fries,et al.  Assessing Neuronal Coherence with Single-Unit, Multi-Unit, and Local Field Potentials , 2006, Neural Computation.

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