Comparison of spatial integration and surround suppression characteristics in spiking activity and the local field potential in macaque V1

Neurons in primary visual cortex exhibit well documented centre–surround receptive field organization, whereby the centre is dominated by excitatory influences and the surround is generally dominated by inhibitory influences. These effects have largely been established by measuring the output of neurons, i.e. their spiking activity. How excitation and inhibition are reflected in the local field potential (LFP) is little understood. As this can bear on the interpretation of human fMRI BOLD data and on our understanding of the mechanisms of local field potential oscillations, we measured spatial integration and centre–surround properties in single‐ and multiunit recordings of V1 in the awake fixating macaque monkey, and compared these to spectral power in different frequency bands of simultaneously recorded LFPs. We quantified centre–surround organization by determining the size of the summation and suppression area in spiking activity as well as in different frequency bands of the LFP, with the main focus on the gamma band. Gratings extending beyond the summation area usually inhibited spiking activity while the LFP gamma‐band activity increased monotonically for all grating sizes. This increase was maximal for stimuli infringing upon the near classical receptive field surround, where suppression started to dominate spiking activity. Thus, suppressive influences in primary cortex can be inferred from spiking activity, but they also seem to affect specific features of gamma‐band LFP activity.

[1]  D. Whitteridge,et al.  The representation of the visual field on the cerebral cortex in monkeys , 1961, The Journal of physiology.

[2]  C. Blakemore,et al.  The neural mechanism of binocular depth discrimination , 1967, The Journal of physiology.

[3]  D. Hubel,et al.  Receptive fields and functional architecture of monkey striate cortex , 1968, The Journal of physiology.

[4]  D. Hubel,et al.  Sequence regularity and geometry of orientation columns in the monkey striate cortex , 1974, The Journal of comparative neurology.

[5]  L. Maffei,et al.  The unresponsive regions of visual cortical receptive fields , 1976, Vision Research.

[6]  S. Sherman,et al.  Receptive-field characteristics of neurons in cat striate cortex: Changes with visual field eccentricity. , 1976, Journal of neurophysiology.

[7]  J. Nelson,et al.  Orientation-selective inhibition from beyond the classic visual receptive field , 1978, Brain Research.

[8]  D. Mackay,et al.  Modulatory influences of moving textured backgrounds on responsiveness of simple cells in feline striate cortex , 1981, The Journal of physiology.

[9]  J. Allman,et al.  Stimulus specific responses from beyond the classical receptive field: neurophysiological mechanisms for local-global comparisons in visual neurons. , 1985, Annual review of neuroscience.

[10]  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.

[11]  E. Switkes,et al.  Functional anatomy of macaque striate cortex. III. Color , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[12]  E. Switkes,et al.  Functional anatomy of macaque striate cortex. II. Retinotopic organization , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[13]  W. Singer,et al.  Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties , 1989, Nature.

[14]  I. Módy,et al.  Halothane enhances tonic neuronal inhibition of elevating intracellular calcium , 1991, Brain Research.

[15]  Rodney J. Douglas,et al.  Synchronization of Bursting Action Potential Discharge in a Model Network of Neocortical Neurons , 1991, Neural Computation.

[16]  T. Wiesel,et al.  Targets of horizontal connections in macaque primary visual cortex , 1991, The Journal of comparative neurology.

[17]  N L Harrison,et al.  Effects of volatile anesthetics on the kinetics of inhibitory postsynaptic currents in cultured rat hippocampal neurons. , 1993, Journal of neurophysiology.

[18]  I. Ohzawa,et al.  Spatiotemporal organization of simple-cell receptive fields in the cat's striate cortex. I. General characteristics and postnatal development. , 1993, Journal of neurophysiology.

[19]  C. Li,et al.  Extensive integration field beyond the classical receptive field of cat's striate cortical neurons--classification and tuning properties. , 1994, Vision research.

[20]  R. Frostig,et al.  Cortical point-spread function and long-range lateral interactions revealed by real-time optical imaging of macaque monkey primary visual cortex , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[21]  I. Ohzawa,et al.  Length and width tuning of neurons in the cat's primary visual cortex. , 1994, Journal of neurophysiology.

[22]  A. Burkhalter,et al.  Evidence for Excitatory Amino Acid Neurotransmitters in Forward and Feedback Corticocortical Pathways within Rat Visual Cortex , 1994, The European journal of neuroscience.

[23]  M. Carandini,et al.  Summation and division by neurons in primate visual cortex. , 1994, Science.

[24]  Roman Bauer,et al.  Different rules of spatial summation from beyond the receptive field for spike rates and oscillation amplitudes in cat visual cortex , 1995, Brain Research.

[25]  G. Orban,et al.  Shape and Spatial Distribution of Receptive Fields and Antagonistic Motion Surrounds in the Middle Temporal Area (V5) of the Macaque , 1995, The European journal of neuroscience.

[26]  W. Singer,et al.  Stimulus dependent intercolumnar synchronization of single unit responses in cat area 17. , 1995, Neuroreport.

[27]  C. Gilbert,et al.  Long-range horizontal connections and their role in cortical reorganization revealed by optical recording of cat primary visual cortex , 1995, Nature.

[28]  C. Gray,et al.  Chattering Cells: Superficial Pyramidal Neurons Contributing to the Generation of Synchronous Oscillations in the Visual Cortex , 1996, Science.

[29]  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.

[30]  A. Burkhalter,et al.  Different Balance of Excitation and Inhibition in Forward and Feedback Circuits of Rat Visual Cortex , 1996, The Journal of Neuroscience.

[31]  G. Buzsáki,et al.  Gamma Oscillation by Synaptic Inhibition in a Hippocampal Interneuronal Network Model , 1996, The Journal of Neuroscience.

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

[33]  W. Singer,et al.  Stimulus-dependent synchronization of neuronal responses in the visual cortex of the awake macaque monkey , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[34]  D. Heeger,et al.  Linear Systems Analysis of Functional Magnetic Resonance Imaging in Human V1 , 1996, The Journal of Neuroscience.

[35]  G. Buzsáki,et al.  Analysis of gamma rhythms in the rat hippocampus in vitro and in vivo. , 1996, The Journal of physiology.

[36]  K. Hoffmann,et al.  Synchronization of Neuronal Activity during Stimulus Expectation in a Direction Discrimination Task , 1997, The Journal of Neuroscience.

[37]  Wolf Singer,et al.  Neuronal Synchrony: A Versatile Code for the Definition of Relations? , 1999, Neuron.

[38]  R. Shapley,et al.  Contrast's effect on spatial summation by macaque V1 neurons , 1999, Nature Neuroscience.

[39]  V. Bringuier,et al.  Horizontal propagation of visual activity in the synaptic integration field of area 17 neurons. , 1999, Science.

[40]  S. Hestrin,et al.  A network of fast-spiking cells in the neocortex connected by electrical synapses , 1999, Nature.

[41]  A. Burkhalter,et al.  Role of GABAB receptor-mediated inhibition in reciprocal interareal pathways of rat visual cortex. , 1999, Journal of neurophysiology.

[42]  W. Singer,et al.  Precisely Synchronized Oscillatory Firing Patterns Require Electroencephalographic Activation , 1999, The Journal of Neuroscience.

[43]  Karl J. Friston,et al.  A direct quantitative relationship between the functional properties of human and macaque V5 , 2000, Nature Neuroscience.

[44]  C. Gilbert,et al.  Spatial distribution of contextual interactions in primary visual cortex and in visual perception. , 2000, Journal of neurophysiology.

[45]  P. Somogyi,et al.  Proximally targeted GABAergic synapses and gap junctions synchronize cortical interneurons , 2000, Nature Neuroscience.

[46]  C. Gray,et al.  Dynamics of striate cortical activity in the alert macaque: I. Incidence and stimulus-dependence of gamma-band neuronal oscillations. , 2000, Cerebral cortex.

[47]  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.

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

[49]  N. Logothetis,et al.  Neurophysiological investigation of the basis of the fMRI signal , 2001, Nature.

[50]  R. Shapley,et al.  Visual spatial characterization of macaque V1 neurons. , 2001, Journal of neurophysiology.

[51]  A. Sillito,et al.  Surround suppression in primate V1. , 2001, Journal of neurophysiology.

[52]  J. B. Levitt,et al.  The spatial extent over which neurons in macaque striate cortex pool visual signals , 2002, Visual Neuroscience.

[53]  N. Logothetis The neural basis of the blood-oxygen-level-dependent functional magnetic resonance imaging signal. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[54]  J. B. Levitt,et al.  Anatomical origins of the classical receptive field and modulatory surround field of single neurons in macaque visual cortical area V1. , 2002, Progress in brain research.

[55]  B. Connors,et al.  The Spatial Dimensions of Electrically Coupled Networks of Interneurons in the Neocortex , 2002, The Journal of Neuroscience.

[56]  J. Movshon,et al.  Nature and interaction of signals from the receptive field center and surround in macaque V1 neurons. , 2002, Journal of neurophysiology.

[57]  Bijan Pesaran,et al.  Temporal structure in neuronal activity during working memory in macaque parietal cortex , 2000, Nature Neuroscience.

[58]  A. Thiele,et al.  Neuronal synchrony does not correlate with motion coherence in cortical area MT , 2003, Nature.

[59]  J. Movshon,et al.  Time Course and Time-Distance Relationships for Surround Suppression in Macaque V1 Neurons , 2003, The Journal of Neuroscience.

[60]  David J Heeger,et al.  Response Suppression in V1 Agrees with Psychophysics of Surround Masking , 2003, The Journal of Neuroscience.

[61]  Andrew T. Smith,et al.  Surround modulation measured with functional MRI in the human visual cortex. , 2003, Journal of neurophysiology.

[62]  Miles A Whittington,et al.  Interneuron Diversity series: Inhibitory interneurons and network oscillations in vitro , 2003, Trends in Neurosciences.

[63]  Xiao-Jing Wang,et al.  What determines the frequency of fast network oscillations with irregular neural discharges? I. Synaptic dynamics and excitation-inhibition balance. , 2003, Journal of neurophysiology.

[64]  Nicholas V. Swindale,et al.  Coverage and the design of striate cortex , 1991, Biological Cybernetics.

[65]  Dario L. Ringach,et al.  Reverse correlation in neurophysiology , 2004, Cogn. Sci..

[66]  Victor A. F. Lamme,et al.  Synchrony and covariation of firing rates in the primary visual cortex during contour grouping , 2004, Nature Neuroscience.

[67]  Paul H. E. Tiesinga,et al.  Rapid Temporal Modulation of Synchrony by Competition in Cortical Interneuron Networks , 2004, Neural Computation.

[68]  R. Vautin,et al.  Magnification factor and receptive field size in foveal striate cortex of the monkey , 2004, Experimental Brain Research.

[69]  R. Eckhorn,et al.  Coherent oscillations: A mechanism of feature linking in the visual cortex? , 1988, Biological Cybernetics.

[70]  G. Buzsáki Large-scale recording of neuronal ensembles , 2004, Nature Neuroscience.

[71]  H. Markram,et al.  Interneurons of the neocortical inhibitory system , 2004, Nature Reviews Neuroscience.

[72]  R. Eckhorn,et al.  Perception-related modulations of local field potential power and coherence in primary visual cortex of awake monkey during binocular rivalry. , 2004, Cerebral cortex.

[73]  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.

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

[75]  P. König,et al.  A comparison of hemodynamic and neural responses in cat visual cortex using complex stimuli. , 2004, Cerebral cortex.

[76]  N. Logothetis,et al.  Neural basis of the blood-oxygen-level-dependent functional magnetic resonance imaging , 2004 .

[77]  G. DeAngelis,et al.  Does Neuronal Synchrony Underlie Visual Feature Grouping? , 2005, Neuron.

[78]  A. Thiele,et al.  Acetylcholine dynamically controls spatial integration in marmoset primary visual cortex. , 2005, Journal of neurophysiology.

[79]  D. McCormick,et al.  Inhibitory Postsynaptic Potentials Carry Synchronized Frequency Information in Active Cortical Networks , 2005, Neuron.

[80]  I. Fried,et al.  Coupling Between Neuronal Firing, Field Potentials, and fMRI in Human Auditory Cortex , 2005, Science.

[81]  R. Andersen,et al.  Cortical Local Field Potential Encodes Movement Intentions in the Posterior Parietal Cortex , 2005, Neuron.

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

[83]  W. Singer,et al.  Hemodynamic Signals Correlate Tightly with Synchronized Gamma Oscillations , 2005, Science.

[84]  S. Hestrin,et al.  Electrical synapses define networks of neocortical GABAergic neurons , 2005, Trends in Neurosciences.

[85]  N. Logothetis,et al.  Local field potential reflects perceptual suppression in monkey visual cortex , 2006, Proceedings of the National Academy of Sciences.

[86]  R. Desimone,et al.  Gamma-band synchronization in visual cortex predicts speed of change detection , 2006, Nature.

[87]  A. Thiele,et al.  A novel electrode–pipette design for simultaneous recording of extracellular spikes and iontophoretic drug application in awake behaving monkeys , 2006, Journal of Neuroscience Methods.

[88]  Contrast-dependent spatial integration in awake macaque V1 measured by fMRI , 2006 .

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

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

[91]  I. Fried,et al.  Coupling between Neuronal Firing Rate, Gamma LFP, and BOLD fMRI Is Related to Interneuronal Correlations , 2007, Current Biology.

[92]  Robert Miller,et al.  Theory of the normal waking EEG: from single neurones to waveforms in the alpha, beta and gamma frequency ranges. , 2007, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[93]  A. Thiele,et al.  Attention alters spatial integration in macaque V1 in an eccentricity-dependent manner , 2007, Nature Neuroscience.

[94]  L. Schwabe,et al.  Response facilitation from the "suppressive" receptive field surround of macaque V1 neurons. , 2007, Journal of neurophysiology.