Frequency-Dependent Attentional Modulation of Local Field Potential Signals in Macaque Area MT

Visual attention modulates neuronal responses in primate motion processing area MT. However, whether it modulates the strength local field potentials (LFP-power) within this area remains unexplored, as well as how this modulation relates to the one of the neurons' response. We investigated these issues by simultaneously recording LFPs and neuronal responses evoked by moving random dot patterns of varying direction and contrast in area MT of two male monkeys (Macaca mulatta) during different behavioral conditions. We found that: (1) LFP-power in the γ (30–120 Hz), but not in the δ (2–4 Hz), θ (4–8 Hz), α (8–12 Hz), β1 (12–20 Hz), and β2 (20–30 Hz) frequency bands, was tuned for motion direction and contrast, similarly to the neurons' response, (2) shifting attention into a neuron's receptive field (RF) decreased LFP-power in the bands below 30 Hz (except the θ band), whereas shifting attention to a stimulus motion direction outside the RF had no effect in these bands, (3) LFP-power in the γ band, however, exhibited both spatial- and motion direction-dependent attentional modulation (increase or decrease), which was highly correlated with the modulation of the neurons' response. These results demonstrate that in area MT, shifting attention into the RFs of neurons in the vicinity of the recording electrode, or to the direction of a moving stimulus located far away from these RFs, distinctively modulates LFP-power in the various frequency bands. They further suggest differences in the neural mechanisms underlying these types of attentional modulation of visual processing.

[1]  S. Zeki.  The response properties of cells in the middle temporal area (area MT) of owl monkey visual cortex , 1980, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[2]  E. Miller,et al.  Serial, Covert Shifts of Attention during Visual Search Are Reflected by the Frontal Eye Fields and Correlated with Population Oscillations , 2009, Neuron.

[3]  D. Bradley,et al.  Structure and function of visual area MT. , 2005, Annual review of neuroscience.

[4]  D. Heeger,et al.  The Normalization Model of Attention , 2009, Neuron.

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

[6]  Arthur Gretton,et al.  Low-Frequency Local Field Potentials and Spikes in Primary Visual Cortex Convey Independent Visual Information , 2008, The Journal of Neuroscience.

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

[8]  W. Newsome,et al.  Local Field Potential in Cortical Area MT: Stimulus Tuning and Behavioral Correlations , 2006, The Journal of Neuroscience.

[9]  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.

[10]  Paul S Khayat,et al.  Attention Differentially Modulates Similar Neuronal Responses Evoked by Varying Contrast and Direction Stimuli in Area MT , 2010, The Journal of Neuroscience.

[11]  S. Treue,et al.  Feature-Based Attention Increases the Selectivity of Population Responses in Primate Visual Cortex , 2004, Current Biology.

[12]  Roman Bauer,et al.  Fast oscillations display sharper orientation tuning than slower components of the same recordings in striate cortex of the awake monkey , 2000, The European journal of neuroscience.

[13]  John J. Foxe,et al.  Increases in alpha oscillatory power reflect an active retinotopic mechanism for distracter suppression during sustained visuospatial attention. , 2006, Journal of neurophysiology.

[14]  Stefan Treue,et al.  Temporal dynamics of neuronal modulation during exogenous and endogenous shifts of visual attention in macaque area MT , 2008, Proceedings of the National Academy of Sciences.

[15]  Christoph Kayser,et al.  Stimulus locking and feature selectivity prevail in complementary frequency ranges of V1 local field potentials , 2004, The European journal of neuroscience.

[16]  R Eckhorn,et al.  Inhibition of sustained gamma oscillations (35-80 Hz) by fast transient responses in cat visual cortex. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[17]  G. Buzsáki.  Theta Oscillations in the Hippocampus , 2002, Neuron.

[18]  Stefan Treue,et al.  Feature-based attention influences motion processing gain in macaque visual cortex , 1999, Nature.

[19]  E. Seidemann,et al.  Effect of spatial attention on the responses of area MT neurons. , 1999, Journal of neurophysiology.

[20]  R. Shapley,et al.  LFP power spectra in V1 cortex: the graded effect of stimulus contrast. , 2005, Journal of neurophysiology.

[21]  U. Mitzdorf.  Properties of the evoked potential generators: current source-density analysis of visually evoked potentials in the cat cortex. , 1987, The International journal of neuroscience.

[22]  N. Logothetis.  The Underpinnings of the BOLD Functional Magnetic Resonance Imaging Signal , 2003, The Journal of Neuroscience.

[23]  M. Carandini,et al.  Stimulus contrast modulates functional connectivity in visual cortex , 2009, Nature Neuroscience.

[24]  G. Karmos,et al.  Entrainment of Neuronal Oscillations as a Mechanism of Attentional Selection , 2008, Science.

[25]  G Karmos.  Oscillatory Entrainment as a Mechanism of Attentional Operation , 2008 .

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

[27]  M. Berger,et al.  High Gamma Power Is Phase-Locked to Theta Oscillations in Human Neocortex , 2006, Science.

[28]  D. J. Felleman,et al.  Receptive-field properties of neurons in middle temporal visual area (MT) of owl monkeys. , 1984, Journal of neurophysiology.

[29]  Christopher C. Pack,et al.  Pattern Motion Selectivity of Spiking Outputs and Local Field Potentials in Macaque Visual Cortex , 2009, The Journal of Neuroscience.

[30]  M. Carandini,et al.  Local Origin of Field Potentials in Visual Cortex , 2009, Neuron.

[31]  Robert Desimone,et al.  Parallel and Serial Neural Mechanisms for Visual Search in Macaque Area V4 , 2005, Science.

[32]  T. Sejnowski,et al.  Cortical Enlightenment: Are Attentional Gamma Oscillations Driven by ING or PING? , 2009, Neuron.

[33]  R. Vogels,et al.  Effects of adaptation on the stimulus selectivity of macaque inferior temporal spiking activity and local field potentials. , 2010, Cerebral cortex.

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

[35]  A. Pérez-Villalba.  Rhythms of the Brain, G. Buzsáki. Oxford University Press, Madison Avenue, New York (2006), Price: GB £42.00, p. 448, ISBN: 0-19-530106-4 , 2008 .

[36]  W. Freiwald,et al.  Coherent oscillatory activity in monkey area v4 predicts successful allocation of attention. , 2005, Cerebral cortex.

[37]  R. Desimone,et al.  The Effects of Visual Stimulation and Selective Visual Attention on Rhythmic Neuronal Synchronization in Macaque Area V4 , 2008, The Journal of Neuroscience.

[38]  N. Logothetis,et al.  Very slow activity fluctuations in monkey visual cortex: implications for functional brain imaging. , 2003, Cerebral cortex.

[39]  Ankoor S. Shah,et al.  An oscillatory hierarchy controlling neuronal excitability and stimulus processing in the auditory cortex. , 2005, Journal of neurophysiology.

[40]  Nikos K Logothetis,et al.  Interpreting the BOLD signal. , 2004, Annual review of physiology.

[41]  U. Mitzdorf.  Current source-density method and application in cat cerebral cortex: investigation of evoked potentials and EEG phenomena. , 1985, Physiological reviews.

[42]  C. Schroeder,et al.  The Gamma Oscillation: Master or Slave? , 2009, Brain Topography.

[43]  Adriano B. L. Tort,et al.  Theta–gamma coupling increases during the learning of item–context associations , 2009, Proceedings of the National Academy of Sciences.

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

[45]  John J. Foxe,et al.  The strength of anticipatory spatial biasing predicts target discrimination at attended locations: a high‐density EEG study , 2009, The European journal of neuroscience.

[46]  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.

[47]  T. Poggio,et al.  Object Selectivity of Local Field Potentials and Spikes in the Macaque Inferior Temporal Cortex , 2006, Neuron.

[48]  W. Klimesch,et al.  Control mechanisms in working memory: A possible function of EEG theta oscillations , 2010, Neuroscience & Biobehavioral Reviews.

[49]  S. Treue,et al.  Attentional Modulation Strength in Cortical Area MT Depends on Stimulus Contrast , 2002, Neuron.

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

[51]  John H. R. Maunsell,et al.  Coding of image contrast in central visual pathways of the macaque monkey , 1990, Vision Research.

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

[53]  John H. R. Maunsell,et al.  Attentional modulation of visual motion processing in cortical areas MT and MST , 1996, Nature.

[54]  Alexander S. Ecker,et al.  Feature Selectivity of the Gamma-Band of the Local Field Potential in Primate Primary Visual Cortex , 2008, Front. Neurosci..