Gamma coherence mediates interhemispheric integration during multiple object tracking

Our ability to track the paths of multiple visual objects moving between the hemifields requires effective integration of information between the two cerebral hemispheres. Coherent neural oscillations in the gamma band (35–70 Hz) are hypothesised to drive this information transfer. Here we manipulated the need for interhemispheric integration using a novel multiple object tracking (MOT) task in which stimuli either moved between the two visual hemifields—requiring interhemispheric integration—or moved within separate visual hemifields. We used electroencephalography (EEG) to measure interhemispheric coherence during the task. Human observers (21 female; 20 male) were poorer at tracking objects between-versus within-hemifields, reflecting a cost of interhemispheric integration. Critically, gamma coherence was greater in trials requiring interhemispheric integration, particularly between sensors over parieto-occipital areas. In approximately half of the participants, the observed cost of integration was associated with a failure of the cerebral hemispheres to become coherent in the gamma band. Moreover, individual differences in this integration cost correlated with endogenous gamma coherence at these same sensors, though with generally opposing relationships for the real and imaginary part of coherence. The real part (capturing synchronisation with a near-zero phase-lag) benefited between-hemifield tracking; imaginary coherence was detrimental. Finally, instantaneous phase-coherence over the tracking period uniquely predicted between-hemifield tracking performance, suggesting that effective integration benefits from sustained interhemispheric synchronisation. Our results show that gamma coherence mediates interhemispheric integration during MOT, and add to a growing body of work demonstrating that coherence drives communication across cortically distributed neural networks.

[1]  D. Kiper,et al.  Visual stimulus-dependent changes in interhemispheric EEG coherence in ferrets. , 1999, Journal of neurophysiology.

[2]  Wolf Singer,et al.  Interhemispheric Connections Shape Subjective Experience of Bistable Motion , 2011, Current Biology.

[3]  M. Hallett,et al.  Identifying true brain interaction from EEG data using the imaginary part of coherency , 2004, Clinical Neurophysiology.

[4]  J Bullier,et al.  Structural basis of cortical synchronization. II. Effects of cortical lesions. , 1995, Journal of neurophysiology.

[5]  H. Kennedy,et al.  Visual Areas Exert Feedforward and Feedback Influences through Distinct Frequency Channels , 2014, Neuron.

[6]  J. Mattingley,et al.  No Evidence for Phase-Specific Effects of 40 Hz HD–tACS on Multiple Object Tracking , 2018, Front. Psychol..

[7]  W. Singer,et al.  Interhemispheric synchronization of oscillatory neuronal responses in cat visual cortex , 1991, Science.

[8]  M. Ding,et al.  Decomposing Neural Synchrony: Toward an Explanation for Near-Zero Phase-Lag in Cortical Oscillatory Networks , 2008, PloS one.

[9]  R. Traub,et al.  A mechanism for generation of long-range synchronous fast oscillations in the cortex , 1996, Nature.

[10]  R. Oostenveld,et al.  Nonparametric statistical testing of EEG- and MEG-data , 2007, Journal of Neuroscience Methods.

[11]  P. Fries Rhythms for Cognition: Communication through Coherence , 2015, Neuron.

[12]  Andreas K. Engel,et al.  Different coupling modes mediate cortical cross-frequency interactions , 2015, NeuroImage.

[13]  W. Singer,et al.  Visuomotor integration is associated with zero time-lag synchronization among cortical areas , 1997, Nature.

[14]  György Buzsáki,et al.  What does gamma coherence tell us about inter-regional neural communication? , 2015, Nature Neuroscience.

[15]  F. Tong,et al.  Neural mechanisms of object-based attention. , 2015, Cerebral cortex.

[16]  F. Varela,et al.  Perception's shadow: long-distance synchronization of human brain activity , 1999, Nature.

[17]  Pascal Fries,et al.  Communication through coherence with inter-areal delays , 2015, Current Opinion in Neurobiology.

[18]  Leonardo L. Gollo,et al.  Dynamical relaying can yield zero time lag neuronal synchrony despite long conduction delays , 2008, Proceedings of the National Academy of Sciences.

[19]  R. Eckhorn,et al.  Stimulus-specific fast oscillations at zero phase between visual areas V1 and V2 of awake monkey. , 1994, Neuroreport.

[20]  Martin V. Sale,et al.  Current challenges: the ups and downs of tACS , 2019, Experimental Brain Research.

[21]  I. Nelken,et al.  Transient Induced Gamma-Band Response in EEG as a Manifestation of Miniature Saccades , 2008, Neuron.

[22]  J. Martinerie,et al.  The brainweb: Phase synchronization and large-scale integration , 2001, Nature Reviews Neuroscience.

[23]  A. von Stein,et al.  Different frequencies for different scales of cortical integration: from local gamma to long range alpha/theta synchronization. , 2000, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[24]  Steven L Franconeri,et al.  Selecting and tracking multiple objects. , 2015, Wiley interdisciplinary reviews. Cognitive science.

[25]  G. Buzsáki,et al.  Neuronal Oscillations in Cortical Networks , 2004, Science.

[26]  M. Lotze,et al.  Brain activation during spatial updating and attentive tracking of moving targets , 2012, Brain and Cognition.

[27]  W. Singer,et al.  Neural Synchrony in Cortical Networks: History, Concept and Current Status , 2009, Front. Integr. Neurosci..

[28]  A. Engel,et al.  Selective Modulation of Interhemispheric Functional Connectivity by HD-tACS Shapes Perception , 2014, PLoS biology.

[29]  Shigeki Nakauchi,et al.  Hemifield Crossings during Multiple Object Tracking Affect Task Performance and Steady-State Visual Evoked Potentials , 2019, Neuroscience.

[30]  Lars T. Westlye,et al.  Functional connectivity indicates differential roles for the intraparietal sulcus and the superior parietal lobule in multiple object tracking , 2015, NeuroImage.

[31]  Erkki Oja,et al.  Independent component analysis: algorithms and applications , 2000, Neural Networks.

[32]  Patrick Cavanagh,et al.  Within-Hemifield Competition in Early Visual Areas Limits the Ability to Track Multiple Objects with Attention , 2014, The Journal of Neuroscience.

[33]  E. Vogel,et al.  Neural Measures of Individual Differences in Selecting and Tracking Multiple Moving Objects , 2008, The Journal of Neuroscience.

[34]  F. Varela,et al.  Measuring phase synchrony in brain signals , 1999, Human brain mapping.

[35]  Christian Büchel,et al.  Neural Coupling Binds Visual Tokens to Moving Stimuli , 2005, The Journal of Neuroscience.

[36]  Guido Nolte,et al.  Spectral fingerprints of large‐scale cortical dynamics during ambiguous motion perception , 2016, Human brain mapping.

[37]  Christian M. Stoppel,et al.  Spatio-temporal Patterns of Brain Activity Distinguish Strategies of Multiple-object Tracking , 2014, Journal of Cognitive Neuroscience.

[38]  R. Sekuler,et al.  EEG Correlates of Attentional Load during Multiple Object Tracking , 2011, PloS one.

[39]  D. Glaser,et al.  Metastable motion anisotropy , 1991, Visual Neuroscience.

[40]  J. Martinerie,et al.  Comparison of Hilbert transform and wavelet methods for the analysis of neuronal synchrony , 2001, Journal of Neuroscience Methods.

[41]  J. Wolfe,et al.  Using Fmri to Distinguish Components of the Multiple Object Tracking Task , 1994 .

[42]  Karl J. Friston,et al.  Zero-lag synchronous dynamics in triplets of interconnected cortical areas , 2001, Neural Networks.

[43]  W. Singer,et al.  Modulation of Neuronal Interactions Through Neuronal Synchronization , 2007, Science.

[44]  H. Jasper,et al.  The ten-twenty electrode system of the International Federation. The International Federation of Clinical Neurophysiology. , 1999, Electroencephalography and clinical neurophysiology. Supplement.

[45]  P. Fries A mechanism for cognitive dynamics: neuronal communication through neuronal coherence , 2005, Trends in Cognitive Sciences.

[46]  T. Womelsdorf,et al.  Attentional Stimulus Selection through Selective Synchronization between Monkey Visual Areas , 2012, Neuron.

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

[48]  P. Cavanagh,et al.  Independent Resources for Attentional Tracking in the Left and Right Visual Hemifields , 2005, Psychological science.

[49]  Roger W Strong,et al.  Hemifield-specific information is exchanged as targets move between the hemifields , 2019 .

[50]  P. Cavanagh,et al.  Tracking multiple targets with multifocal attention , 2005, Trends in Cognitive Sciences.

[51]  Toralf Neuling,et al.  Friends, not foes: Magnetoencephalography as a tool to uncover brain dynamics during transcranial alternating current stimulation , 2015, NeuroImage.

[52]  T. Sejnowski,et al.  Correlated neuronal activity and the flow of neural information , 2001, Nature Reviews Neuroscience.

[53]  C. Elger,et al.  Human memory formation is accompanied by rhinal–hippocampal coupling and decoupling , 2001, Nature Neuroscience.

[54]  Hans-Jochen Heinze,et al.  Neural correlates of multiple object tracking strategies , 2015, NeuroImage.

[55]  George A. Alvarez,et al.  Hemifield-specific control mechanisms for spatial working memory and attention: evidence from hemifield crossover costs. , 2018 .

[56]  Arnaud Delorme,et al.  EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis , 2004, Journal of Neuroscience Methods.

[57]  M. Siegel,et al.  Dissociating neuronal gamma-band activity from cranial and ocular muscle activity in EEG , 2013, Front. Hum. Neurosci..

[58]  A. Engel,et al.  Spectral fingerprints of large-scale neuronal interactions , 2012, Nature Reviews Neuroscience.

[59]  A. Engel,et al.  Antiphasic 40 Hz Oscillatory Current Stimulation Affects Bistable Motion Perception , 2013, Brain Topography.

[60]  W. Drongelen,et al.  Localization of brain electrical activity via linearly constrained minimum variance spatial filtering , 1997, IEEE Transactions on Biomedical Engineering.

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

[62]  Søren K. Andersen,et al.  Sustained Multifocal Attentional Enhancement of Stimulus Processing in Early Visual Areas Predicts Tracking Performance , 2013, The Journal of Neuroscience.