Laminar analysis of visually evoked activity in the primary visual cortex

Studying the laminar pattern of neural activity is crucial for understanding the processing of neural signals in the cerebral cortex. We measured neural population activity [multiunit spike activity (MUA) and local field potential, LFP] in Macaque primary visual cortex (V1) in response to drifting grating stimuli. Sustained visually driven MUA was at an approximately constant level across cortical depth in V1. However, sustained, visually driven, local field potential power, which was concentrated in the γ-band (20–60 Hz), was greatest at the cortical depth corresponding to cortico-cortical output layers 2, 3, and 4B. γ-band power also tends to be more sustained in the output layers. Overall, cortico-cortical output layers accounted for 67% of total γ-band activity in V1, whereas 56% of total spikes evoked by drifting gratings were from layers 2, 3, and 4B. The high-resolution layer specificity of γ-band power, the laminar distribution of MUA and γ-band activity, and their dynamics imply that neural activity in V1 is generated by laminar-specific mechanisms. In particular, visual responses of MUA and γ-band activity in cortico-cortical output layers 2, 3, and 4B seem to be strongly influenced by laminar-specific recurrent circuitry and/or feedback.

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

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

[3]  Alexander Maier,et al.  Infragranular Sources of Sustained Local Field Potential Responses in Macaque Primary Visual Cortex , 2011, The Journal of Neuroscience.

[4]  R. Desimone,et al.  Laminar differences in gamma and alpha coherence in the ventral stream , 2011, Proceedings of the National Academy of Sciences.

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

[6]  P. König,et al.  A Functional Gamma-Band Defined by Stimulus-Dependent Synchronization in Area 18 of Awake Behaving Cats , 2003, The Journal of Neuroscience.

[7]  M. A. Smith,et al.  Stimulus Selectivity and Spatial Coherence of Gamma Components of the Local Field Potential , 2011, The Journal of Neuroscience.

[8]  R. Shapley,et al.  “Black” Responses Dominate Macaque Primary Visual Cortex V1 , 2009, The Journal of Neuroscience.

[9]  Nancy Kopell,et al.  Gamma Oscillations and Stimulus Selection , 2008, Neural Computation.

[10]  R. Eckhorn,et al.  Contour decouples gamma activity across texture representation in monkey striate cortex. , 2000, Cerebral cortex.

[11]  C. Schroeder,et al.  The Leading Sense: Supramodal Control of Neurophysiological Context by Attention , 2009, Neuron.

[12]  J. Maunsell,et al.  Differences in Gamma Frequencies across Visual Cortex Restrict Their Possible Use in Computation , 2010, Neuron.

[13]  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.

[14]  Nicholas J. Priebe,et al.  Inhibition, Spike Threshold, and Stimulus Selectivity in Primary Visual Cortex , 2008, Neuron.

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

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

[17]  Louise S. Delicato,et al.  Attention Reduces Stimulus-Driven Gamma Frequency Oscillations and Spike Field Coherence in V1 , 2010, Neuron.

[18]  Michael Okun,et al.  The Subthreshold Relation between Cortical Local Field Potential and Neuronal Firing Unveiled by Intracellular Recordings in Awake Rats , 2010, The Journal of Neuroscience.

[19]  R. Shapley,et al.  Spatial Spread of the Local Field Potential and its Laminar Variation in Visual Cortex , 2009, The Journal of Neuroscience.

[20]  R. Shapley,et al.  A Dynamic Nonlinearity and Spatial Phase Specificity in Macaque V1 Neurons , 2007, The Journal of Neuroscience.

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

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

[23]  Judith A Hirsch,et al.  Laminar processing in the visual cortical column , 2006, Current Opinion in Neurobiology.

[24]  P. Somogyi,et al.  Salient features of synaptic organisation in the cerebral cortex 1 Published on the World Wide Web on 3 March 1998. 1 , 1998, Brain Research Reviews.

[25]  J. B. Levitt,et al.  Comparison of intrinsic connectivity in different areas of macaque monkey cerebral cortex. , 1993, Cerebral cortex.

[26]  R. Yuste,et al.  Dense, Unspecific Connectivity of Neocortical Parvalbumin-Positive Interneurons: A Canonical Microcircuit for Inhibition? , 2011, The Journal of Neuroscience.

[27]  C. Schroeder,et al.  A spatiotemporal profile of visual system activation revealed by current source density analysis in the awake macaque. , 1998, Cerebral cortex.

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

[29]  A. Grinvald,et al.  Relationship between intrinsic connections and functional architecture revealed by optical imaging and in vivo targeted biocytin injections in primate striate cortex. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[30]  J. B. Levitt,et al.  Circuits for Local and Global Signal Integration in Primary Visual Cortex , 2002, The Journal of Neuroscience.

[31]  M. Hawken,et al.  Laminar organization and contrast sensitivity of direction-selective cells in the striate cortex of the Old World monkey , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[32]  Nikos K Logothetis,et al.  Laminar specificity in monkey V1 using high-resolution SE-fMRI. , 2006, Magnetic resonance imaging.

[33]  R. Shapley,et al.  Generation of Black-Dominant Responses in V1 Cortex , 2010, The Journal of Neuroscience.

[34]  Xiao-Jing Wang Neurophysiological and computational principles of cortical rhythms in cognition. , 2010, Physiological reviews.

[35]  A. Thiele,et al.  Comparison of spatial integration and surround suppression characteristics in spiking activity and the local field potential in macaque V1 , 2008, The European journal of neuroscience.

[36]  R. Douglas,et al.  Recurrent neuronal circuits in the neocortex , 2007, Current Biology.

[37]  R. Shapley,et al.  Orientation Selectivity in Macaque V1: Diversity and Laminar Dependence , 2002, The Journal of Neuroscience.

[38]  W. Singer,et al.  Stimulus‐Dependent Neuronal Oscillations in Cat Visual Cortex: Receptive Field Properties and Feature Dependence , 1990, The European journal of neuroscience.

[39]  Nicole C. Rust,et al.  Do We Know What the Early Visual System Does? , 2005, The Journal of Neuroscience.

[40]  Samuel P. Burns,et al.  Comparisons of the Dynamics of Local Field Potential and Multiunit Activity Signals in Macaque Visual Cortex , 2010, The Journal of Neuroscience.

[41]  N. Logothetis,et al.  From Neurons to Circuits: Linear Estimation of Local Field Potentials , 2009, The Journal of Neuroscience.

[42]  B. McNaughton,et al.  Paradoxical Effects of External Modulation of Inhibitory Interneurons , 1997, The Journal of Neuroscience.

[43]  Michael J. Shelley,et al.  LFP spectral peaks in V1 cortex: network resonance and cortico-cortical feedback , 2010, Journal of Computational Neuroscience.

[44]  G. Buzsáki,et al.  Mechanisms of gamma oscillations. , 2012, Annual review of neuroscience.

[45]  Lawrence C. Sincich,et al.  The circuitry of V1 and V2: integration of color, form, and motion. , 2005, Annual review of neuroscience.

[46]  E. Callaway Local circuits in primary visual cortex of the macaque monkey. , 1998, Annual review of neuroscience.

[47]  Dario L Ringach,et al.  Untuned Suppression Makes a Major Contribution to the Enhancement of Orientation Selectivity in Macaque V1 , 2011, The Journal of Neuroscience.

[48]  Johannes Reichold,et al.  The microvascular system of the striate and extrastriate visual cortex of the macaque. , 2008, Cerebral cortex.

[49]  J. Lund,et al.  Anatomical organization of macaque monkey striate visual cortex. , 1988, Annual review of neuroscience.

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

[51]  L. Abbott,et al.  Divisive inhibition in recurrent networks , 2000, Network.

[52]  Ankoor S. Shah,et al.  Neural dynamics and the fundamental mechanisms of event-related brain potentials. , 2004, Cerebral cortex.

[53]  Chun-I Yeh,et al.  On and off domains of geniculate afferents in cat primary visual cortex , 2008, Nature Neuroscience.