Effective Connectivity of Depth-Structure–Selective Patches in the Lateral Bank of the Macaque Intraparietal Sulcus

Extrastriate cortical areas are frequently composed of subpopulations of neurons encoding specific features or stimuli, such as color, disparity, or faces, and patches of neurons encoding similar stimulus properties are typically embedded in interconnected networks, such as the attention or face-processing network. The goal of the current study was to examine the effective connectivity of subsectors of neurons in the same cortical area with highly similar neuronal response properties. We first recorded single- and multi-unit activity to identify two neuronal patches in the anterior part of the macaque intraparietal sulcus (IPS) showing the same depth structure selectivity and then employed electrical microstimulation during functional magnetic resonance imaging in these patches to determine the effective connectivity of these patches. The two IPS subsectors we identified—with the same neuronal response properties and in some cases separated by only 3 mm—were effectively connected to remarkably distinct cortical networks in both dorsal and ventral stream in three macaques. Conversely, the differences in effective connectivity could account for the known visual-to-motor gradient within the anterior IPS. These results clarify the role of the anterior IPS as a pivotal brain region where dorsal and ventral visual stream interact during object analysis. Thus, in addition to the anatomical connectivity of cortical areas and the properties of individual neurons in these areas, the effective connectivity provides novel key insights into the widespread functional networks that support behavior.

[1]  Guy A. Orban,et al.  Monkey Cortex through fMRI Glasses , 2014, Neuron.

[2]  Stefan Everling,et al.  Distinct and distributed functional connectivity patterns across cortex reflect the domain-specific constraints of object, face, scene, body, and tool category-selective modules in the ventral visual pathway , 2014, NeuroImage.

[3]  Ivo D. Popivanov,et al.  Probabilistic and Single-Subject Retinotopic Maps Reveal the Topographic Organization of Face Patches in the Macaque Cortex , 2014, The Journal of Neuroscience.

[4]  Maria C Romero,et al.  Coding of Shape Features in the Macaque Anterior Intraparietal Area , 2014, The Journal of Neuroscience.

[5]  Anna W Roe,et al.  Optical imaging of cortical networks via intracortical microstimulation. , 2013, Journal of neurophysiology.

[6]  Liam D. Kaufman,et al.  Human fMRI Reveals That Delayed Action Re-Recruits Visual Perception , 2013, PloS one.

[7]  Maria Alessandra Umiltà,et al.  Somato-Motor Haptic Processing in Posterior Inner Perisylvian Region (SII/pIC) of the Macaque Monkey , 2013, PloS one.

[8]  J. Gore,et al.  The Relationship of Anatomical and Functional Connectivity to Resting-State Connectivity in Primate Somatosensory Cortex , 2013, Neuron.

[9]  Sabine Kastner,et al.  The representation of tool and non-tool object information in the human intraparietal sulcus. , 2013, Journal of neurophysiology.

[10]  G. Luppino,et al.  Connectional heterogeneity of the ventral part of the macaque area 46. , 2013, Cerebral cortex.

[11]  Pierpaolo Pani,et al.  Three-dimensional Shape Coding in Grasping Circuits: A Comparison between the Anterior Intraparietal Area and Ventral Premotor Area F5a , 2013, Journal of Cognitive Neuroscience.

[12]  Peter Janssen,et al.  FEF-microstimulation causes task-dependent modulation of occipital fMRI activity , 2013, NeuroImage.

[13]  Peter Janssen,et al.  The Role of Binocular Disparity in Stereoscopic Images of Objects in the Macaque Anterior Intraparietal Area , 2013, PloS one.

[14]  Ilse C. L. Van Dromme,et al.  The relation between single-cell activity and fMRI activations in posterior parietal cortex , 2012 .

[15]  Pierpaolo Pani,et al.  Selectivity for Three-Dimensional Shape and Grasping-Related Activity in the Macaque Ventral Premotor Cortex , 2012, The Journal of Neuroscience.

[16]  Bruce R. Rosen,et al.  Optogenetically Induced Behavioral and Functional Network Changes in Primates , 2012, Current Biology.

[17]  Bruce G Cumming,et al.  Decision-related activity in sensory neurons: correlations among neurons and with behavior. , 2012, Annual review of neuroscience.

[18]  Maria C Romero,et al.  Responses to two‐dimensional shapes in the macaque anterior intraparietal area , 2012, The European journal of neuroscience.

[19]  Yong Gu,et al.  Causal Links between Dorsal Medial Superior Temporal Area Neurons and Multisensory Heading Perception , 2012, The Journal of Neuroscience.

[20]  R. Vogels,et al.  Inferotemporal Cortex Subserves Three-Dimensional Structure Categorization , 2012, Neuron.

[21]  Yasushi Miyashita,et al.  Direct comparison of spontaneous functional connectivity and effective connectivity measured by intracortical microstimulation: an fMRI study in macaque monkeys. , 2011, Cerebral cortex.

[22]  W. Vanduffel,et al.  Functional Heterogeneity of Macaque Lateral Intraparietal Neurons , 2011, The Journal of Neuroscience.

[23]  L. Fogassi,et al.  Decoding the activity of grasping neurons recorded from the ventral premotor area F5 of the macaque monkey , 2011, Neuroscience.

[24]  Alexander Kraskov,et al.  Ventral Premotor–Motor Cortex Interactions in the Macaque Monkey during Grasp: Response of Single Neurons to Intracortical Microstimulation , 2011, The Journal of Neuroscience.

[25]  Wim Vanduffel,et al.  Grasping-Related Functional Magnetic Resonance Imaging Brain Responses in the Macaque Monkey , 2011, The Journal of Neuroscience.

[26]  Karl J. Friston Functional and Effective Connectivity: A Review , 2011, Brain Connect..

[27]  Peter Janssen,et al.  Synchronization between the end stages of the dorsal and the ventral visual stream. , 2011, Journal of neurophysiology.

[28]  M. Pinsk,et al.  Visuotopic Organization of Macaque Posterior Parietal Cortex: A Functional Magnetic Resonance Imaging Study , 2011, The Journal of Neuroscience.

[29]  G. Luppino,et al.  Cortical connections of the anterior (F5a) subdivision of the macaque ventral premotor area F5 , 2011, Brain Structure and Function.

[30]  Guy A. Orban,et al.  The Selectivity of Neurons in the Macaque Fundus of the Superior Temporal Area for Three-Dimensional Structure from Motion , 2010, The Journal of Neuroscience.

[31]  N. Logothetis,et al.  The effects of electrical microstimulation on cortical signal propagation , 2010, Nature Neuroscience.

[32]  H. Sakata,et al.  Functional and histological properties of caudal intraparietal area of macaque monkey , 2010, Neuroscience.

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

[34]  G. Luppino,et al.  Cortical connections of the macaque caudal ventrolateral prefrontal areas 45A and 45B. , 2010, Cerebral cortex.

[35]  G. Orban,et al.  The Representation of Tool Use in Humans and Monkeys: Common and Uniquely Human Features , 2009, The Journal of Neuroscience.

[36]  Peter Janssen,et al.  A Distinct Representation of Three-Dimensional Shape in Macaque Anterior Intraparietal Area: Fast, Metric, and Coarse , 2009, The Journal of Neuroscience.

[37]  Guy A. Orban,et al.  The monkey ventral premotor cortex processes 3D shape from disparity , 2009, NeuroImage.

[38]  W. Vanduffel,et al.  Visual Field Map Clusters in Macaque Extrastriate Visual Cortex , 2009, The Journal of Neuroscience.

[39]  Hansjörg Scherberger,et al.  Context-Specific Grasp Movement Representation in the Macaque Anterior Intraparietal Area , 2009, The Journal of Neuroscience.

[40]  Jody C. Culham,et al.  Ventral and dorsal stream contributions to the online control of immediate and delayed grasping: A TMS approach , 2009, Neuropsychologia.

[41]  Svetlana S. Georgieva,et al.  The Processing of Three-Dimensional Shape from Disparity in the Human Brain , 2009, The Journal of Neuroscience.

[42]  Eric T. Carlson,et al.  A neural code for three-dimensional object shape in macaque inferotemporal cortex , 2008, Nature Neuroscience.

[43]  P. Roelfsema,et al.  Bottom-Up Dependent Gating of Frontal Signals in Early Visual Cortex , 2008, Science.

[44]  N. Logothetis What we can do and what we cannot do with fMRI , 2008, Nature.

[45]  Doris Y. Tsao,et al.  Patches with Links: A Unified System for Processing Faces in the Macaque Temporal Lobe , 2008, Science.

[46]  A. Murata,et al.  Cortical connections of the macaque anterior intraparietal (AIP) area. , 2008, Cerebral cortex.

[47]  Jody C. Culham,et al.  Does tool-related fMRI activity within the intraparietal sulcus reflect the plan to grasp? , 2007, NeuroImage.

[48]  Peter Janssen,et al.  Anterior Regions of Monkey Parietal Cortex Process Visual 3D Shape , 2007, Neuron.

[49]  Michael L. Platt,et al.  Neural correlates of reward and attention in macaque area LIP , 2006, Neuropsychologia.

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

[51]  L. Fogassi,et al.  Functional properties of grasping-related neurons in the ventral premotor area F5 of the macaque monkey. , 2006, Journal of neurophysiology.

[52]  E. J. Tehovnik,et al.  Mapping Cortical Activity Elicited with Electrical Microstimulation Using fMRI in the Macaque , 2005, Neuron.

[53]  Dottie M. Clower,et al.  Basal ganglia and cerebellar inputs to 'AIP'. , 2005, Cerebral cortex.

[54]  M. Shadlen,et al.  A representation of the hazard rate of elapsed time in macaque area LIP , 2005, Nature Neuroscience.

[55]  T. Moore,et al.  Microstimulation of the frontal eye field and its effects on covert spatial attention. , 2004, Journal of neurophysiology.

[56]  Doris Y. Tsao,et al.  Faces and objects in macaque cerebral cortex , 2003, Nature Neuroscience.

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

[58]  Olivier D. Faugeras,et al.  Flows of diffeomorphisms for multimodal image registration , 2002, Proceedings IEEE International Symposium on Biomedical Imaging.

[59]  G. Orban,et al.  Extracting 3D from Motion: Differences in Human and Monkey Intraparietal Cortex , 2002, Science.

[60]  G. Orban,et al.  Visual Motion Processing Investigated Using Contrast Agent-Enhanced fMRI in Awake Behaving Monkeys , 2001, Neuron.

[61]  H. Sakata,et al.  From Three-Dimensional Space Vision to Prehensile Hand Movements: The Lateral Intraparietal Area Links the Area V3A and the Anterior Intraparietal Area in Macaques , 2001, The Journal of Neuroscience.

[62]  S. Ben Hamed,et al.  Representation of the visual field in the lateral intraparietal area of macaque monkeys: a quantitative receptive field analysis , 2001, Experimental Brain Research.

[63]  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.

[64]  D. V. van Essen,et al.  Mapping of architectonic subdivisions in the macaque monkey, with emphasis on parieto‐occipital cortex , 2000, The Journal of comparative neurology.

[65]  G. Orban,et al.  Selectivity for 3D shape that reveals distinct areas within macaque inferior temporal cortex. , 2000, Science.

[66]  R. Andersen,et al.  Intention-related activity in the posterior parietal cortex: a review , 2000, Vision Research.

[67]  H. Sakata,et al.  Selectivity for the shape, size, and orientation of objects for grasping in neurons of monkey parietal area AIP. , 2000, Journal of neurophysiology.

[68]  A. Nambu,et al.  Organization of nonprimary motor cortical inputs on pyramidal and nonpyramidal tract neurons of primary motor cortex: An electrophysiological study in the macaque monkey. , 2000, Cerebral cortex.

[69]  P. Boesiger,et al.  SENSE: Sensitivity encoding for fast MRI , 1999, Magnetic resonance in medicine.

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

[71]  Michael A. Arbib,et al.  Modeling parietal-premotor interactions in primate control of grasping , 1998, Neural Networks.

[72]  A. Parker,et al.  Sense and the single neuron: probing the physiology of perception. , 1998, Annual review of neuroscience.

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

[74]  J. Bullier,et al.  Functional streams in occipito-frontal connections in the monkey , 1996, Behavioural Brain Research.

[75]  J. Bullier,et al.  Topography of visual cortex connections with frontal eye field in macaque: convergence and segregation of processing streams , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[76]  C. Bruce,et al.  Topography of projections to posterior cortical areas from the macaque frontal eye fields , 1995, The Journal of comparative neurology.

[77]  H. Sakata,et al.  Deficit of hand preshaping after muscimol injection in monkey parietal cortex , 1994, Neuroreport.

[78]  D. J. Felleman,et al.  Distributed hierarchical processing in the primate cerebral cortex. , 1991, Cerebral cortex.

[79]  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.

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