On the Role of the Inferior Intraparietal Sulcus in Visual Working Memory for Lateralized Single-feature Objects

A consolidated practice in cognitive neuroscience is to explore the properties of human visual working memory through the analysis of electromagnetic signals using cued change detection tasks. Under these conditions, EEG/MEG activity increments in the posterior parietal cortex scaling with the number of memoranda are often reported in the hemisphere contralateral to the objects' position in the memory array. This highly replicable finding clashes with several reported failures to observe compatible hemodynamic activity modulations using fMRI or fNIRS in comparable tasks. Here, we reconcile this apparent discrepancy by acquiring fMRI data on healthy participants and employing a cluster analysis to group voxels in the posterior parietal cortex based on their functional response. The analysis identified two distinct subpopulations of voxels in the intraparietal sulcus (IPS) showing a consistent functional response among participants. One subpopulation, located in the superior IPS, showed a bilateral response to the number of objects coded in visual working memory. A different subpopulation, located in the inferior IPS, showed an increased unilateral response when the objects were displayed contralaterally. The results suggest that a cluster of neurons in the inferior IPS is a candidate source of electromagnetic contralateral responses to working memory load in cued change detection tasks.

[1]  C. Frith,et al.  The Role of Working Memory in Visual Selective Attention , 2001, Science.

[2]  D. Louis Collins,et al.  Symmetric Atlasing and Model Based Segmentation: An Application to the Hippocampus in Older Adults , 2006, MICCAI.

[3]  S. Kastner,et al.  Shifting Attentional Priorities: Control of Spatial Attention through Hemispheric Competition , 2013, The Journal of Neuroscience.

[4]  S. Yantis,et al.  Transient neural activity in human parietal cortex during spatial attention shifts , 2002, Nature Neuroscience.

[5]  M. Chun,et al.  Dissociable neural mechanisms supporting visual short-term memory for objects , 2006, Nature.

[6]  D. Gitelman,et al.  Neuroanatomic Overlap of Working Memory and Spatial Attention Networks: A Functional MRI Comparison within Subjects , 1999, NeuroImage.

[7]  Bruce Fischl,et al.  Accurate and robust brain image alignment using boundary-based registration , 2009, NeuroImage.

[8]  E. Vogel,et al.  Contralateral delay activity provides a neural measure of the number of representations in visual working memory. , 2010, Journal of neurophysiology.

[9]  M. Corbetta,et al.  Neural basis and recovery of spatial attention deficits in spatial neglect , 2005, Nature Neuroscience.

[10]  Leslie G. Ungerleider,et al.  Transient and sustained activity in a distributed neural system for human working memory , 1997, Nature.

[11]  C. Kennard,et al.  Human Medial Frontal Cortex Mediates Unconscious Inhibition of Voluntary Action , 2007, Neuron.

[12]  S. Luck,et al.  Electrophysiological correlates of feature analysis during visual search. , 1994, Psychophysiology.

[13]  Edward K. Vogel,et al.  Neural Measures of Dynamic Changes in Attentive Tracking Load , 2012, Journal of Cognitive Neuroscience.

[14]  Joachim M. Buhmann,et al.  Stability-Based Validation of Clustering Solutions , 2004, Neural Computation.

[15]  Alfonso Caramazza,et al.  Temporal Brain Dynamics of Multiple Object Processing: The Flexibility of Individuation , 2011, PloS one.

[16]  Patrik Pluchino,et al.  A hemodynamic correlate of lateralized visual short-term memories , 2011, Neuropsychologia.

[17]  Benoit Brisson,et al.  Dissociation of the N2pc and sustained posterior contralateral negativity in a choice response task , 2008, Brain Research.

[18]  Stephen M Smith,et al.  Fast robust automated brain extraction , 2002, Human brain mapping.

[19]  S. Kastner,et al.  Mechanisms of Spatial Attention Control in Frontal and Parietal Cortex , 2010, The Journal of Neuroscience.

[20]  Wolf Singer,et al.  Gamma-Band Activity in Human Prefrontal Cortex Codes for the Number of Relevant Items Maintained in Working Memory , 2012, The Journal of Neuroscience.

[21]  D. Somers,et al.  Hemispheric Asymmetry in Visuotopic Posterior Parietal Cortex Emerges with Visual Short-Term Memory Load , 2010, The Journal of Neuroscience.

[22]  A. A. Wijers,et al.  An event-related brain potential correlate of visual short-term memory. , 1999, Neuroreport.

[23]  Nicolas Robitaille,et al.  Distinguishing between lateralized and nonlateralized brain activity associated with visual short-term memory: fMRI, MEG, and EEG evidence from the same observers , 2010, NeuroImage.

[24]  S J Luck,et al.  Spatial filtering during visual search: evidence from human electrophysiology. , 1994, Journal of experimental psychology. Human perception and performance.

[25]  Ferath Kherif,et al.  Distributed cell assemblies for general lexical and category‐specific semantic processing as revealed by fMRI cluster analysis , 2009, Human brain mapping.

[26]  Michael Erb,et al.  Dynamical Cluster Analysis of Cortical fMRI Activation , 1999, NeuroImage.

[27]  G. Seber Multivariate observations / G.A.F. Seber , 1983 .

[28]  R. Malach,et al.  Data-driven clustering reveals a fundamental subdivision of the human cortex into two global systems , 2008, Neuropsychologia.

[29]  Steven J. Luck,et al.  The Allocation of Attention and Working Memory in Visual Crowding , 2015, Journal of Cognitive Neuroscience.

[30]  Nikolaus Weiskopf,et al.  Optimal EPI parameters for reduction of susceptibility-induced BOLD sensitivity losses: A whole-brain analysis at 3 T and 1.5 T , 2006, NeuroImage.

[31]  Michael Brady,et al.  Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images , 2002, NeuroImage.

[32]  Leslie G. Ungerleider,et al.  Neural Correlates of Visual Working Memory fMRI Amplitude Predicts Task Performance , 2002, Neuron.

[33]  Christian N L Olivers,et al.  Interactions between visual working memory and visual attention. , 2008, Frontiers in bioscience : a journal and virtual library.

[34]  Stephen M. Emrich,et al.  Visual Search Elicits the Electrophysiological Marker of Visual Working Memory , 2009, PloS one.

[35]  Edward Awh,et al.  The contralateral delay activity as a neural measure of visual working memory , 2016, Neuroscience & Biobehavioral Reviews.

[36]  Daniel J. Mitchell,et al.  Flexible, capacity-limited activity of posterior parietal cortex in perceptual as well as visual short-term memory tasks. , 2008, Cerebral cortex.

[37]  Jöran Lepsien,et al.  Directing spatial attention in mental representations: Interactions between attentional orienting and working-memory load , 2005, NeuroImage.

[38]  Ryan Mruczek,et al.  Intraparietal regions play a material general role in working memory: Evidence supporting an internal attentional role , 2015, Neuropsychologia.

[39]  A. Nobre,et al.  Where and When to Pay Attention: The Neural Systems for Directing Attention to Spatial Locations and to Time Intervals as Revealed by Both PET and fMRI , 1998, The Journal of Neuroscience.

[40]  N. Cowan The magical number 4 in short-term memory: A reconsideration of mental storage capacity , 2001, Behavioral and Brain Sciences.

[41]  David J. Prime,et al.  Inability to suppress salient distractors predicts low visual working memory capacity , 2016, Proceedings of the National Academy of Sciences.

[42]  Richard O. Duda,et al.  Pattern classification and scene analysis , 1974, A Wiley-Interscience publication.

[43]  Jason B Mattingley,et al.  Distributed and Overlapping Neural Substrates for Object Individuation and Identification in Visual Short-Term Memory. , 2014, Cerebral cortex.

[44]  Anna C. Nobre,et al.  Spatial Attention can Bias Search in Visual Short-Term Memory , 2007, Frontiers in human neuroscience.

[45]  Edward E. Smith,et al.  Temporal dynamics of brain activation during a working memory task , 1997, Nature.

[46]  Glyn W. Humphreys,et al.  The Left Intraparietal Sulcus Modulates the Selection of Low Salient Stimuli , 2009, Journal of Cognitive Neuroscience.

[47]  J. Jonides,et al.  Overlapping mechanisms of attention and spatial working memory , 2001, Trends in Cognitive Sciences.

[48]  E. Vogel,et al.  Capacity limit of visual short-term memory in human posterior parietal cortex , 2004 .

[49]  J. Schall,et al.  Executive control of countermanding saccades by the supplementary eye field , 2006, Nature Neuroscience.

[50]  P. Maquet,et al.  Orienting Attention to Locations in Perceptual Versus Mental Representations , 2004, Journal of Cognitive Neuroscience.

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

[52]  L. K. Hansen,et al.  On Clustering fMRI Time Series , 1999, NeuroImage.

[53]  J. Schall,et al.  Performance monitoring by the supplementary eye ® eld , 2000 .

[54]  Mircea Ariel Schoenfeld,et al.  Neural sources of visual working memory maintenance in human parietal and ventral extrastriate visual cortex , 2015, NeuroImage.

[55]  M. Eimer The N2pc component as an indicator of attentional selectivity. , 1996, Electroencephalography and clinical neurophysiology.

[56]  Mark W. Woolrich,et al.  FSL , 2012, NeuroImage.

[57]  Carmel Mevorach,et al.  Ignoring the Elephant in the Room: A Neural Circuit to Downregulate Salience , 2010, The Journal of Neuroscience.

[58]  Jean-Francois Mangin,et al.  Automatized clustering and functional geometry of human parietofrontal networks for language, space, and number , 2004, NeuroImage.

[59]  Roy Luria,et al.  Orienting attention to objects in visual short-term memory , 2009, Neuropsychologia.

[60]  Edward K. Vogel,et al.  Come Together, Right Now: Dynamic Overwriting of an Object's History through Common Fate , 2014, Journal of Cognitive Neuroscience.

[61]  Veronica Mazza,et al.  Individuation of multiple targets during visual enumeration: New insights from electrophysiology , 2012, Neuropsychologia.

[62]  E. Vogel,et al.  Working memory and fluid intelligence: Capacity, attention control, and secondary memory retrieval , 2014, Cognitive Psychology.

[63]  Maro G. Machizawa,et al.  Neural activity predicts individual differences in visual working memory capacity , 2004, Nature.

[64]  Edward Awh,et al.  Working Memory Delay Activity Predicts Individual Differences in Cognitive Abilities , 2015, Journal of Cognitive Neuroscience.

[65]  Lotfi B Merabet,et al.  Visual Topography of Human Intraparietal Sulcus , 2007, The Journal of Neuroscience.

[66]  Jöran Lepsien,et al.  Searching for Targets within the Spatial Layout of Visual Short-Term Memory , 2009, The Journal of Neuroscience.

[67]  Michael W. Cole,et al.  Canceling planned action: an FMRI study of countermanding saccades. , 2004, Cerebral cortex.

[68]  A. Bowman,et al.  Applied smoothing techniques for data analysis : the kernel approach with S-plus illustrations , 1999 .

[69]  Roy Luria,et al.  Visual Short-term Memory Capacity for Simple and Complex Objects , 2010, Journal of Cognitive Neuroscience.

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

[71]  E. Vogel,et al.  Visual working memory capacity: from psychophysics and neurobiology to individual differences , 2013, Trends in Cognitive Sciences.

[72]  Maro G. Machizawa,et al.  Neural measures reveal individual differences in controlling access to working memory , 2005, Nature.

[73]  T. Braver,et al.  Cognitive Neuroscience Approaches to Individual Differences in Working Memory and Executive Control: Conceptual and Methodological Issues , 2010 .

[74]  R. Dell’Acqua,et al.  The Demonstration of Short-Term Consolidation , 1998, Cognitive Psychology.