Visual Contrast Sensitivity Improvement by Right Frontal High-Beta Activity Is Mediated by Contrast Gain Mechanisms and Influenced by Fronto-Parietal White Matter Microstructure.

Behavioral and electrophysiological studies in humans and non-human primates have correlated frontal high-beta activity with the orienting of endogenous attention and shown the ability of the latter function to modulate visual performance. We here combined rhythmic transcranial magnetic stimulation (TMS) and diffusion imaging to study the relation between frontal oscillatory activity and visual performance, and we associated these phenomena to a specific set of white matter pathways that in humans subtend attentional processes. High-beta rhythmic activity on the right frontal eye field (FEF) was induced with TMS and its causal effects on a contrast sensitivity function were recorded to explore its ability to improve visual detection performance across different stimulus contrast levels. Our results show that frequency-specific activity patterns engaged in the right FEF have the ability to induce a leftward shift of the psychometric function. This increase in visual performance across different levels of stimulus contrast is likely mediated by a contrast gain mechanism. Interestingly, microstructural measures of white matter connectivity suggest a strong implication of right fronto-parietal connectivity linking the FEF and the intraparietal sulcus in propagating high-beta rhythmic signals across brain networks and subtending top-down frontal influences on visual performance.

[1]  R. Desimone,et al.  Attention Increases Sensitivity of V4 Neurons , 2000, Neuron.

[2]  Robert M. Mok,et al.  Causal implication by rhythmic transcranial magnetic stimulation of alpha frequency in feature‐based local vs. global attention , 2012, The European journal of neuroscience.

[3]  M. Landy,et al.  The effect of viewpoint on perceived visual roughness. , 2007, Journal of vision.

[4]  T. Paus,et al.  Transcranial Magnetic Stimulation of the Human Frontal Eye Field: Effects on Visual Perception and Attention , 2002, Journal of Cognitive Neuroscience.

[5]  J. Giedd Structural Magnetic Resonance Imaging of the Adolescent Brain , 2004, Annals of the New York Academy of Sciences.

[6]  Michelle K. Jetha,et al.  Electrophysiological changes during adolescence: A review , 2010, Brain and Cognition.

[7]  Romain Quentin,et al.  Fronto-Parietal Anatomical Connections Influence the Modulation of Conscious Visual Perception by High-Beta Frontal Oscillatory Activity. , 2015, Cerebral cortex.

[8]  Stefan Treue,et al.  Different populations of neurons contribute to the detection and discrimination of visual motion , 2001, Vision Research.

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

[10]  T. Gasser,et al.  Development of the EEG of school-age children and adolescents. II. Topography. , 1988, Electroencephalography and clinical neurophysiology.

[11]  G. V. Simpson,et al.  Parieto‐occipital ∼1 0Hz activity reflects anticipatory state of visual attention mechanisms , 1998 .

[12]  M. Catani,et al.  Can spherical deconvolution provide more information than fiber orientations? Hindrance modulated orientational anisotropy, a true‐tract specific index to characterize white matter diffusion , 2013, Human brain mapping.

[13]  J. H. Steiger Tests for comparing elements of a correlation matrix. , 1980 .

[14]  M. Massimini,et al.  Natural Frequencies of Human Corticothalamic Circuits , 2009, The Journal of Neuroscience.

[15]  Á. Pascual-Leone,et al.  α-Band Electroencephalographic Activity over Occipital Cortex Indexes Visuospatial Attention Bias and Predicts Visual Target Detection , 2006, The Journal of Neuroscience.

[16]  T. Ergenoğlu,et al.  Alpha rhythm of the EEG modulates visual detection performance in humans. , 2004, Brain research. Cognitive brain research.

[17]  Catherine Tallon-Baudry,et al.  Causal Frequency-Specific Contributions of Frontal Spatiotemporal Patterns Induced by Non-Invasive Neurostimulation to Human Visual Performance , 2013, The Journal of Neuroscience.

[18]  P. Roelfsema,et al.  Modulation of the Contrast Response Function by Electrical Microstimulation of the Macaque Frontal Eye Field , 2009, The Journal of Neuroscience.

[19]  M. Corbetta,et al.  Control of goal-directed and stimulus-driven attention in the brain , 2002, Nature Reviews Neuroscience.

[20]  P. Schyns,et al.  Rhythmic TMS Causes Local Entrainment of Natural Oscillatory Signatures , 2011, Current Biology.

[21]  G. Boynton,et al.  Global effects of feature-based attention in human visual cortex , 2002, Nature Neuroscience.

[22]  A. Nobre,et al.  Indexing the graded allocation of visuospatial attention using anticipatory alpha oscillations , 2011, Journal of neurophysiology.

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

[24]  Steven Phillips,et al.  Greater frontal-parietal synchrony at low gamma-band frequencies for inefficient than efficient visual search in human EEG. , 2009, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[25]  C. Herrmann,et al.  Transcranial Alternating Current Stimulation Enhances Individual Alpha Activity in Human EEG , 2010, PloS one.

[26]  Paolo Bartolomeo,et al.  Dorsal and Ventral Parietal Contributions to Spatial Orienting in the Human Brain , 2011, The Journal of Neuroscience.

[27]  M. Corbetta,et al.  The Reorienting System of the Human Brain: From Environment to Theory of Mind , 2008, Neuron.

[28]  Matthew F Glasser,et al.  DTI tractography of the human brain's language pathways. , 2008, Cerebral cortex.

[29]  T. Paus Location and function of the human frontal eye-field: A selective review , 1996, Neuropsychologia.

[30]  C. Herrmann,et al.  Neural synchrony and white matter variations in the human brain--relation between evoked γ frequency and corpus callosum morphology. , 2011, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[31]  Giorgio Fuggetta,et al.  Modulation of cortical oscillatory activities induced by varying single-pulse transcranial magnetic stimulation intensity over the left primary motor area: A combined EEG and TMS study , 2005, NeuroImage.

[32]  G. Edelman,et al.  A measure for brain complexity: relating functional segregation and integration in the nervous system. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[33]  M. Carrasco,et al.  A population-coding model of attention’s influence on contrast response: Estimating neural effects from psychophysical data , 2009, Vision Research.

[34]  Romain Quentin,et al.  Fronto-tectal white matter connectivity mediates facilitatory effects of non-invasive neurostimulation on visual detection , 2013, NeuroImage.

[35]  Manuel Schabus,et al.  A shift of visual spatial attention is selectively associated with human EEG alpha activity , 2005, The European journal of neuroscience.

[36]  Giuseppe Scotti,et al.  A modified damped Richardson–Lucy algorithm to reduce isotropic background effects in spherical deconvolution , 2010, NeuroImage.

[37]  Roberto Hornero,et al.  The correlation between white-matter microstructure and the complexity of spontaneous brain activity: A difussion tensor imaging-MEG study , 2011, NeuroImage.

[38]  David M. Groppe,et al.  Mass univariate analysis of event-related brain potentials/fields I: a critical tutorial review. , 2011, Psychophysiology.

[39]  Abbas F. Sadikot,et al.  The neural response to transcranial magnetic stimulation of the human motor cortex. II. Thalamocortical contributions , 2006, Experimental Brain Research.

[40]  C. Tyler,et al.  Bayesian adaptive estimation of psychometric slope and threshold , 1999, Vision Research.

[41]  R. Deichmann,et al.  Concurrent TMS-fMRI and Psychophysics Reveal Frontal Influences on Human Retinotopic Visual Cortex , 2006, Current Biology.

[42]  A. Karim,et al.  Brain Oscillatory Substrates of Visual Short-Term Memory Capacity , 2009, Current Biology.

[43]  J. Reynolds,et al.  Attentional modulation of visual processing. , 2004, Annual review of neuroscience.

[44]  M. Catani,et al.  A lateralized brain network for visuospatial attention , 2011, Nature Neuroscience.

[45]  Romain Quentin,et al.  Manipulation of Pre-Target Activity on the Right Frontal Eye Field Enhances Conscious Visual Perception in Humans , 2012, PloS one.

[46]  Romain Quentin,et al.  Frontal eye field, where art thou? Anatomy, function, and non-invasive manipulation of frontal regions involved in eye movements and associated cognitive operations , 2014, Front. Integr. Neurosci..

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

[48]  Tomáš Paus,et al.  The neural response to transcranial magnetic stimulation of the human motor cortex. I. Intracortical and cortico-cortical contributions , 2006, Experimental Brain Research.

[49]  P. J. Basser,et al.  Role of myelin plasticity in oscillations and synchrony of neuronal activity , 2014, Neuroscience.

[50]  J. Gross,et al.  On the Role of Prestimulus Alpha Rhythms over Occipito-Parietal Areas in Visual Input Regulation: Correlation or Causation? , 2010, The Journal of Neuroscience.

[51]  M. Carrasco,et al.  Attention alters appearance , 2004, Nature Neuroscience.

[52]  R. Desimone,et al.  The Role of Neural Mechanisms of Attention in Solving the Binding Problem , 1999, Neuron.

[53]  M. Carrasco,et al.  How do attention and adaptation affect contrast sensitivity? , 2007, Journal of vision.

[54]  Gregor Thut,et al.  Rhythmic TMS over Parietal Cortex Links Distinct Brain Frequencies to Global versus Local Visual Processing , 2011, Current Biology.

[55]  Tomás Paus,et al.  Transcranial Magnetic Stimulation of the Human Frontal Eye ®eld Facilitates Visual Awareness , 2022 .

[56]  M. Carrasco,et al.  Sustained and transient covert attention enhance the signal via different contrast response functions , 2006, Vision Research.

[57]  N. Prins Psychophysics: A Practical Introduction , 2009 .

[58]  Miles A. Whittington,et al.  Neurosystems: brain rhythms and cognitive processing , 2013, The European journal of neuroscience.

[59]  G. V. Simpson,et al.  Anticipatory Biasing of Visuospatial Attention Indexed by Retinotopically Specific α-Bank Electroencephalography Increases over Occipital Cortex , 2000, The Journal of Neuroscience.

[60]  T. Gasser,et al.  Development of the EEG of school-age children and adolescents. I. Analysis of band power. , 1988, Electroencephalography and clinical neurophysiology.