Occipital Alpha and Gamma Oscillations Support Complementary Mechanisms for Processing Stimulus Value Associations

Selective attention is reflected neurally in changes in the power of posterior neural oscillations in the alpha (8–12 Hz) and gamma (40–100 Hz) bands. Although a neural mechanism that allows relevant information to be selectively processed has its advantages, it may lead to lucrative or dangerous information going unnoticed. Neural systems are also in place for processing rewarding and punishing information. Here, we examine the interaction between selective attention (left vs. right) and stimulus's learned value associations (neutral, punished, or rewarded) and how they compete for control of posterior neural oscillations. We found that both attention and stimulus–value associations influenced neural oscillations. Whereas selective attention had comparable effects on alpha and gamma oscillations, value associations had dissociable effects on these neural markers of attention. Salient targets (associated with positive and negative outcomes) hijacked changes in alpha power—increasing hemispheric alpha lateralization when salient targets were attended, decreasing it when they were being ignored. In contrast, hemispheric gamma-band lateralization was specifically abolished by negative distractors. Source analysis indicated occipital generators of both attentional and value effects. Thus, posterior cortical oscillations support both the ability to selectively attend while at the same time retaining the ability to remain sensitive to valuable features in the environment. Moreover, the versatility of our attentional system to respond separately to salient from merely positively valued stimuli appears to be carried out by separate neural processes reflected in different frequency bands.

[1]  J Gross,et al.  REPRINTS , 1962, The Lancet.

[2]  R. Dolan,et al.  Cholinergic Enhancement of Visual Attention and Neural Oscillations in the Human Brain , 2012, Current Biology.

[3]  C. Gerloff,et al.  Spontaneous locally restricted EEG alpha activity determines cortical excitability in the motor cortex , 2009, Neuropsychologia.

[4]  E. Fox,et al.  Facial Expressions of Emotion: Are Angry Faces Detected More Efficiently? , 2000, Cognition & emotion.

[5]  Ole Jensen,et al.  Frontal Eye Fields Control Attentional Modulation of Alpha and Gamma Oscillations in Contralateral Occipitoparietal Cortex , 2015, The Journal of Neuroscience.

[6]  Matthias M. Müller,et al.  Selective Attention to Task-Irrelevant Emotional Distractors Is Unaffected by the Perceptual Load Associated with a Foreground Task , 2012, PloS one.

[7]  Robert Oostenveld,et al.  FieldTrip: Open Source Software for Advanced Analysis of MEG, EEG, and Invasive Electrophysiological Data , 2010, Comput. Intell. Neurosci..

[8]  Robert Oostenveld,et al.  Visual Cortical Gamma-Band Activity During Free Viewing of Natural Images , 2013, Cerebral cortex.

[9]  C. N. Boehler,et al.  The influence of reward associations on conflict processing in the Stroop task , 2010, Cognition.

[10]  S. Muthukumaraswamy The use of magnetoencephalography in the study of psychopharmacology (pharmaco-MEG) , 2014, Journal of psychopharmacology.

[11]  Robert Oostenveld,et al.  Visually induced gamma-band activity predicts speed of change detection in humans , 2010, NeuroImage.

[12]  Marius V Peelen,et al.  Reward guides attention to object categories in real-world scenes. , 2015, Journal of experimental psychology. General.

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

[14]  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.

[15]  R. Hari,et al.  Human cortical oscillations: a neuromagnetic view through the skull , 1997, Trends in Neurosciences.

[16]  J. Schoffelen,et al.  Parieto‐occipital sources account for the increase in alpha activity with working memory load , 2007, Human brain mapping.

[17]  O. Jensen,et al.  Shaping Functional Architecture by Oscillatory Alpha Activity: Gating by Inhibition , 2010, Front. Hum. Neurosci..

[18]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

[19]  Jane E Raymond,et al.  Learned Predictiveness Speeds Visual Processing , 2012, Psychological science.

[20]  Paul Tiesinga,et al.  Oscillatory mechanisms of feedforward and feedback visual processing , 2015, Trends in Neurosciences.

[21]  J. Theeuwes,et al.  Reward grabs the eye: Oculomotor capture by rewarding stimuli , 2012, Vision Research.

[22]  Louise S. Delicato,et al.  Acetylcholine contributes through muscarinic receptors to attentional modulation in V1 , 2008, Nature.

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

[24]  T. Moore,et al.  CONTROL OF VISUAL CORTICAL SIGNALS BY PREFRONTAL DOPAMINE , 2011, Nature.

[25]  O. Jensen,et al.  Alpha Oscillations Serve to Protect Working Memory Maintenance against Anticipated Distracters , 2012, Current Biology.

[26]  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.

[27]  W. Klimesch,et al.  EEG alpha synchronization and functional coupling during top‐down processing in a working memory task , 2005, Human brain mapping.

[28]  John J. Foxe,et al.  Anticipatory Attentional Suppression of Visual Features Indexed by Oscillatory Alpha-Band Power Increases:A High-Density Electrical Mapping Study , 2010, The Journal of Neuroscience.

[29]  Jorge V. José,et al.  Synchronization as a mechanism for attentional gain modulation , 2004, Neurocomputing.

[30]  Patryk A. Laurent,et al.  Value-driven attentional capture , 2011, Proceedings of the National Academy of Sciences.

[31]  Robert Oostenveld,et al.  Real-time MEG neurofeedback training of posterior alpha activity modulates subsequent visual detection performance , 2015, NeuroImage.

[32]  T. Moore,et al.  The role of neuromodulators in selective attention , 2011, Trends in Cognitive Sciences.

[33]  Thomas R Knösche,et al.  Tangential derivative mapping of axial MEG applied to event-related desynchronization research , 2000, Clinical Neurophysiology.

[34]  Robert Oostenveld,et al.  Online and offline tools for head movement compensation in MEG , 2013, NeuroImage.

[35]  Leslie G. Ungerleider,et al.  Increased Activity in Human Visual Cortex during Directed Attention in the Absence of Visual Stimulation , 1999, Neuron.

[36]  Ole Jensen,et al.  Alpha Oscillations Correlate with the Successful Inhibition of Unattended Stimuli , 2011, Journal of Cognitive Neuroscience.

[37]  P. Roelfsema,et al.  Alpha and gamma oscillations characterize feedback and feedforward processing in monkey visual cortex , 2014, Proceedings of the National Academy of Sciences.

[38]  G. A. Miller,et al.  Cross-frequency dynamics of neuromagnetic oscillatory activity: two mechanisms of emotion regulation. , 2012, Psychophysiology.

[39]  Anina N. Rich,et al.  Spatial attention increases high-frequency gamma synchronisation in human medial visual cortex , 2013, NeuroImage.

[40]  C. Pennartz,et al.  A unified selection signal for attention and reward in primary visual cortex , 2013, Proceedings of the National Academy of Sciences.

[41]  D. Gitelman,et al.  Covert Visual Spatial Orienting and Saccades: Overlapping Neural Systems , 2000, NeuroImage.

[42]  L. Itti,et al.  Mechanisms of top-down attention , 2011, Trends in Neurosciences.

[43]  O. Bertrand,et al.  Oscillatory gamma activity in humans and its role in object representation , 1999, Trends in Cognitive Sciences.

[44]  J. Kaiser,et al.  Human gamma-frequency oscillations associated with attention and memory , 2007, Trends in Neurosciences.

[45]  Henry J. Alitto,et al.  Simultaneous Recordings from the Primary Visual Cortex and Lateral Geniculate Nucleus Reveal Rhythmic Interactions and a Cortical Source for Gamma-Band Oscillations , 2014, The Journal of Neuroscience.

[46]  M. Codispoti,et al.  Affective modulation of the LPP and α-ERD during picture viewing. , 2011, Psychophysiology.

[47]  E. Miller,et al.  Response to Comment on "Top-Down Versus Bottom-Up Control of Attention in the Prefrontal and Posterior Parietal Cortices" , 2007, Science.

[48]  J. Maunsell Neuronal representations of cognitive state: reward or attention? , 2004, Trends in Cognitive Sciences.

[49]  Barbara F. Händel,et al.  Top-Down Controlled Alpha Band Activity in Somatosensory Areas Determines Behavioral Performance in a Discrimination Task , 2011, The Journal of Neuroscience.

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

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

[52]  A. Engel,et al.  Neuronal Synchronization along the Dorsal Visual Pathway Reflects the Focus of Spatial Attention , 2008, Neuron.

[53]  Tom Beesley,et al.  When goals conflict with values: counterproductive attentional and oculomotor capture by reward-related stimuli. , 2015, Journal of experimental psychology. General.

[54]  M. Hasselmo,et al.  Modes and Models of Forebrain Cholinergic Neuromodulation of Cognition , 2011, Neuropsychopharmacology.

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

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

[57]  F. H. Lopes da Silva Neural mechanisms underlying brain waves: from neural membranes to networks. , 1991, Electroencephalography and clinical neurophysiology.

[58]  L. Chelazzi,et al.  Learning to Attend and to Ignore Is a Matter of Gains and Losses , 2009, Psychological science.

[59]  F. Carver,et al.  Visual Awareness, Emotion, and Gamma Band Synchronization , 2008, Cerebral cortex.

[60]  J. Eastwood,et al.  Negative facial expression captures attention and disrupts performance , 2003, Perception & psychophysics.

[61]  G. Underwood,et al.  Salience of the lambs: a test of the saliency map hypothesis with pictures of emotive objects. , 2012, Journal of vision.

[62]  Peter Redgrave,et al.  A computational model of action selection in the basal ganglia. I. A new functional anatomy , 2001, Biological Cybernetics.

[63]  D. Kahneman,et al.  The Boundaries of Loss Aversion , 2005 .

[64]  Y. Saalmann,et al.  The Pulvinar Regulates Information Transmission Between Cortical Areas Based on Attention Demands , 2012, Science.

[65]  L. Chelazzi,et al.  Rewards teach visual selective attention , 2013, Vision Research.

[66]  John T Serences,et al.  Value-Based Modulations in Human Visual Cortex , 2008, Neuron.